Roles of Puf proteins in mRNA degradation and translation

Wiley Interdisciplinary Reviews: RNA

Volumn 2, Issue 4, 2011, Pages 471-492

  Miller, Melanie A ^a   Olivas, Wendy M ^a  

^a UNIVERSITY OF MISSOURI ST LOUIS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; PUF PROTEIN; REGULATOR PROTEIN; UNCLASSIFIED DRUG; MUTANT PROTEIN; RNA BINDING PROTEIN;

3' UNTRANSLATED REGION; BINDING AFFINITY; BIOGENESIS; CELL DIFFERENTIATION; CELL PROLIFERATION; CRYSTAL STRUCTURE; EMBRYO DEVELOPMENT; GENE REPRESSION; HUMAN; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW; RNA BINDING; RNA DEGRADATION; RNA TRANSLATION; SPERMATOGENESIS; TRANSLATION INITIATION; ANIMAL; BIOLOGICAL MODEL; CHEMICAL STRUCTURE; CHEMISTRY; FEMALE; GENETICS; MALE; METABOLISM; NERVOUS SYSTEM DEVELOPMENT; PROTEIN DOMAIN; PROTEIN SYNTHESIS; RNA STABILITY;

EUKARYOTA;

3' UNTRANSLATED REGIONS; ANIMALS; EMBRYONIC DEVELOPMENT; FEMALE; HUMANS; MALE; MODELS, BIOLOGICAL; MODELS, MOLECULAR; MUTANT PROTEINS; NEUROGENESIS; PHENOTYPE; PROTEIN BIOSYNTHESIS; PROTEIN INTERACTION DOMAINS AND MOTIFS; RNA STABILITY; RNA, MESSENGER; RNA-BINDING PROTEINS;

EID: 79960922805     PISSN: 17577004     EISSN: 17577012     Source Type: Journal    
DOI: 10.1002/wrna.69     Document Type: Review

References (127)

1. Shim J, Karin M. The control of mRNA stability in response to extracellular stimuli. Mol Cells 2002, 14:323-331.
2. Kanitz A, Gerber AP. Circuitry of mRNA regulation. WIREs Syst Biol Med 2009, 2:245-251. doi:10.1002/wsbm.55.
3. Mansfield KD, Keene JD. The ribonome: a dominant force in co-ordinating gene expression. Biol Cell 2009, 101:169-181. doi:BC20080055[pii]10.1042/ BC20080055.
4. Wickens M, Bernstein DS, Kimble J, Parker R. A PUF family portrait: 3′UTR regulation as a way of life. Trends Genet 2002, 18:150-157. doi:10.1016/S0168-9525(01)02616-6.
5. Spassov D, Jurecic R. The PUF family of RNA-binding proteins: does evolutionarily conserved structure equal conserved function? IUBMB Life 2003, 55:359-366. doi:10.1080/15216540310001603093.
6. Wharton RP, Aggarwal AK. mRNA regulation by Puf domain proteins. Sci STKE 2006:pe37. doi:10.1126/ stke.3542006pe37.
7. Barker DD, Wang C, Moore J, Dickinson LK, Lehmann R. Pumilio is essential for function but not for distribution of the Drosophila abdominal determinant Nanos. Genes Dev 1992, 6:2312-2326. doi: 10.1101/gad.6.12a.2312.
8. Macdonald PM. The Drosophila pumilio gene: an unusually long transcription unit and an unusual protein. Development 1992, 114:221-232.
9. Zamore PD, Williamson JR, Lehmann R. The Pumilio protein binds RNA through a conserved domain that defines a new class of RNA-binding proteins. RNA 1997, 3:1421-1433.
10. Zhang B, Gallegos M, Puoti A, Durkin E, Fields S, Kimble J, Wickens MP. A conserved RNA-binding protein that regulates sexual fates in the C. elegans hermaphrodite germ line. Nature 1997, 390:477-484. doi:10.1038/37297.
11. White EK, Moore-Jarrett T, Ruley HE. PUM2, a novel murine puf protein, and its consensus RNA-binding site. RNA 2001, 7:1855-1866.
12. Houshmandi SS, Olivas WM. Yeast Puf3 mutants reveal the complexity of Puf-RNA binding and identify a loop required for regulation of mRNA decay. RNA 2005, 11:1655-1666. doi:10.1261/rna.2168505.
13. Spassov DS, Jurecic R. Cloning and comparative sequence analysis of PUM1 and PUM2 genes, human members of the Pumilio family of RNA-binding proteins. Gene 2002, 299:195-204. doi:10.1016/S0378-1119(02)01060-0.
14. Andersson MG, Cerenius L. Pumilio homologue from Saprolegnia parasitica specifically expressed in undifferentiated spore cysts. Eukaryot Cell 2002, 1:105-111. doi:10.1128/EC.1.1.
15. Salvetti A, Rossi L, Lena A, Batistoni R, Deri P, Rainaldi G, Locci MT, Evangelista M, Gremigni V. DjPum, a homologue of Drosophila Pumilio, is essential to planarian stem cell maintenance. Development 2005, 132:1863-1874. doi:10.1242/dev.01785.
16. Nakahata S, Katsu Y, Mita K, Inoue K, Nagahama Y, Yamashita M. Biochemical identification of Xenopus Pumilio as a sequence-specific cyclin B1 mRNA-binding protein that physically interacts with a Nanos homolog, Xcat-2, and a cytoplasmic polyadenylation element-binding protein. J Biol Chem 2001, 276:20945-20953. doi:10.1074/jbc.M010528200.
17. Francischini CW, Quaggio RB. Molecular characterization of Arabidopsis thaliana PUF proteins-binding specificity and target candidates. Febs J 2009, 276: 5456-5470. doi:10.1111/j.1742-4658.2009.07230.x.
18. Dallagiovanna B, Perez L, Sotelo-Silveira J, Smircich P, Duhagon MA, Garat B. Trypanosoma cruzi: molecular characterization of TcPUF6, a Pumilio protein. Exp Parasitol 2005, 109:260-264. doi:10.1016/j.exppara. 2005.01.003.
19. Wharton RP, Sonoda J, Lee T, Patterson M, Murata Y. The Pumilio RNA-binding domain is also a translational regulator. Mol Cell 1998, 1:863-872. doi:10.1016/S1097-2765(00)80085-4.
20. Zamore PD, Bartel DP, Lehmann R, Williamson JR. The PUMILIO-RNA interaction: a single RNA-binding domain monomer recognizes a bipartite target sequence. Biochemistry 1999, 38:596-604. doi:10.1021/bi982264s.
21. Gu W, Deng Y, Zenklusen D, Singer RH. A new yeast PUF family protein, Puf6p, represses ASH1 mRNA translation and is required for its localization. Genes Dev 2004, 18:1452-1465. doi:10.1101/gad.1189004.
22. Jackson JS Jr, Houshmandi SS, Lopez Leban F, Olivas WM. Recruitment of the Puf3 protein to its mRNA target for regulation of mRNA decay in yeast. RNA 2004, 10:1625-1636. doi:10.1261/rna.7270204.
23. Ulbricht RJ, Olivas WM. Puf1p acts in combination with other yeast Puf proteins to control mRNA stability. RNA 2008, 14:246-262. doi:10.1261/rna. 847408.
24. Menon KP, Andrews S, Murthy M, Gavis ER, Zinn K. The translational repressors Nanos and Pumilio have divergent effects on presynaptic terminal growth and postsynaptic glutamate receptor subunit composition. J Neurosci 2009, 29:5558-5572. doi:10.1523/JNEU ROSCI.0520-09.2009.
25. Kadyrova LY, Habara Y, Lee TH, Wharton RP. Translational control of maternal Cyclin B mRNA by Nanos in the Drosophila germline. Development 2007, 134:1519-1527. doi:10.1242/dev.002212.
26. Salazar AM, Silverman EJ, Menon KP, Zinn K. Regulation of synaptic Pumilio function by an aggregation-prone domain. J Neurosci 2010, 30:515-522. doi: 10.1523/JNEUROSCI.2523-09.2010.
27. Spassov DS, Jurecic R. Mouse Pum1 and Pum2 genes, members of the Pumilio family of RNA-binding proteins, show differential expression in fetal and adult hematopoietic stem cells and progenitors. Blood Cells Mol Dis 2003, 30:55-69. doi:10.1016/S1079-9796(03)00003-2.
28. Vessey JP, Vaccani A, Xie Y, Dahm R, Karra D, Kiebler MA, Macchi P. Dendritic localization of the translational repressor Pumilio 2 and its contribution to dendritic stress granules. J Neurosci 2006, 26:6496-6508. doi:10.1523/JNEUROSCI.0649-06. 2006.
29. Kuo MW, Wang SH, Chang JC, Chang CH, Huang LJ, Lin HH, Yu AL, Li WH, Yu J. A novel puf-A gene predicted from evolutionary analysis is involved in the development of eyes and primordial germ-cells. PLoS One 2009, 4:e4980. doi:10.1371/journal.pone. 0004980.
30. Archer SK, Luu VD, de Queiroz RA, Brems S, Clayton C. Trypanosoma brucei PUF9 regulates mRNAs for proteins involved in replicative processes over the cell cycle. PLoS Pathog 2009, 5:e1000565. doi:10.1371/ journal.ppat.1000565.
31. Ariz M, Mainpal R, Subramaniam KC. elegans RNA-binding proteins PUF-8 and MEX-3 function redundantly to promote germline stem cell mitosis. Dev Biol 2009, 326:295-304. doi:10.1016/j.ydbio.2008. 11.024.
32. Crittenden SL, Bernstein DS, Bachorik JL, Thompson BE, Gallegos M, Petcherski AG, Moulder G, Barstead R, Wickens M, Kimble J. A conserved RNA-binding protein controls germline stem cells in Caenorhabditis elegans. Nature 2002, 417:660-663. doi:10.1038/nature754.
33. Garcia-Rodriguez LJ, Gay AC, Pon LA. Puf3p, a Pumilio family RNA binding protein, localizes to mitochondria and regulates mitochondrial biogenesis and motility in budding yeast. J Cell Biol 2007, 176:197-207. doi:10.1083/jcb.200606054.
34. Gerber AP, Herschlag D, Brown PO. Extensive association of functionally and cytotopically related mRNAs with Puf family RNA-binding proteins in yeast. PLoS Biol 2004, 2:E79. doi:10.1371/journal.pbio.0020079.
35. Jaruzelska J, Kotecki M, Kusz K, Spik A, Firpo M, Reijo Pera RA. Conservation of a Pumilio-Nanos complex from Drosophila germ plasm to human germ cells. Dev Genes Evol 2003, 213:120-126. doi:10.1007/ s00427-003-0303-2.
36. Lublin AL, Evans TC. The RNA-binding proteins PUF-5, PUF-6, and PUF-7 reveal multiple systems for maternal mRNA regulation during C. elegans oogenesis. Dev Biol 2007, 303:635-649. doi:10.1016/j.ydbio. 2006.12.004.
37. Menon KP, Sanyal S, Habara Y, Sanchez R, Wharton RP, Ramaswami M, Zinn K. The translational repressor Pumilio regulates presynaptic morphology and controls postsynaptic accumulation of translation factor eIF-4E. Neuron 2004, 44:663-676. doi:10.1016/ j.neuron.2004.10.028.
38. Moore FL, Jaruzelska J, Fox MS, Urano J, Firpo MT, Turek PJ, Dorfman DM, Pera RA. Human Pumilio-2 is expressed in embryonic stem cells and germ cells and interacts with DAZ (Deleted in AZoospermia) and DAZ-like proteins. Proc Natl Acad Sci U S A 2003, 100:538-543. doi:10.1073/pnas.0234478100.
39. Morris AR, Mukherjee N, Keene JD. Ribonomic analysis of human Pum1 reveals cis-trans conservation across species despite evolution of diverse mRNA target sets. Mol Cell Biol 2008, 28:4093-4103. doi: 10.1128/MCB.00155-08.
40. Droll D, Archer S, Fenn K, Delhi P, Matthews K, Clayton C. The trypanosome Pumilio-domain protein PUF7 associates with a nuclear cyclophilin and is involved in ribosomal RNA maturation. FEBS Lett 2010, 584:1156-1162. doi:10.1016/j.febslet.2010. 02.018.
41. Luu VD, Brems S, Hoheisel JD, Burchmore R, Guilbride DL, Clayton C. Functional analysis of Trypanosoma brucei PUF1. Mol Biochem Parasitol 2006, 150:340-349. doi:10.1016/j.molbiopara. 2006.09.007.
42. Dallagiovanna B, Correa A, Probst CM, Holetz F, Smircich P, de Aguiar AM, Mansur F, da Silva CV, Mortara RA, Garat B, et al. Functional genomic characterization of mRNAs associated with TcPUF6, a Pumilio-like protein from Trypanosoma cruzi. J Biol Chem 2008, 283:8266-8273. doi:10.1074/jbc. M703097200.
43. Pique M, Lopez JM, Foissac S, Guigo R, Mendez R. A combinatorial code for CPE-mediated translational control. Cell 2008, 132:434-448. doi:10.1016/ j.cell.2007.12.038.
44. Kaye JA, Rose NC, Goldsworthy B, Goga A, L'Etoile ND. A 3′UTR pumilio-binding element directs translational activation in olfactory sensory neurons. Neuron 2009, 61:57-70. doi:10.1016/j.neuron.2008.11.012.
45. Suh N, Crittenden SL, Goldstrohm A, Hook B, Thompson B, Wickens M, Kimble J. FBF and its dual control of gld-1 expression in the Caenorhabditis elegans germline. Genetics 2009, 181:1249-1260. doi: 10.1534/genetics.108.099440.
46. Schweers BA, Walters KJ, Stern M. The Drosophila melanogaster translational repressor pumilio regulates neuronal excitability. Genetics 2002, 161:1177-1185.
47. Mee CJ, Pym EC, Moffat KG, Baines RA. Regulation of neuronal excitability through pumilio-dependent control of a sodium channel gene. J Neurosci 2004, 24:8695-8703. doi:10.1523/JNEUROSCI.2282-04. 2004.
48. Muraro NI, Weston AJ, Gerber AP, Luschnig S, Moffat KG, Baines RA. Pumilio binds para mRNA and requires Nanos and Brat to regulate sodium current in Drosophila motoneurons. J Neurosci 2008, 28:2099-2109. doi:10.1523/JNEUROSCI.5092-07. 2008.
49. Nolde MJ, Saka N, Reinert KL, Slack FJ. The Caenorhabditis elegans pumilio homolog, puf-9, is required for the 3′UTR-mediated repression of the let-7 microRNA target gene, hbl-1. Dev Biol 2007, 305:551-563. doi:10.1016/j.ydbio.2007.02.040.
50. Vessey JP, Schoderboeck L, Gingi E, Luzi E, Riefler J, Di Leva F, Karra D, Thomas S, Kiebler MA, Macchi P. Mammalian Pumilio 2 regulates dendrite morphogenesis and synaptic function. Proc Natl Acad Sci U S A 2010, 107:3223-3227. doi:10.1073/pnas. 0907128107.
51. Ye B, Petritsch C, Clark IE, Gavis ER, Jan LY, Jan YN. Nanos and Pumilio are essential for dendrite morphogenesis in Drosophila peripheral neurons. Curr Biol 2004, 14:314-321. doi:10.1016/j.cub.2004. 01.052.
52. Wreden C, Verrotti AC, Schisa JA, Lieberfarb ME, Strickland S. Nanos and pumilio establish embryonic polarity in Drosophila by promoting posterior deadenylation of hunchback mRNA. Development 1997, 124:3015-3023.
53. Lehmann R, Nusslein-Volhard C. Involvement of the pumilio gene in the transport of an abdominal signal in the Drosophila embryo. Nature 1987, 329:167-170. doi:10.1038/329167a0.
54. Murata Y, Wharton RP. Binding of pumilio to maternal hunchback mRNA is required for posterior patterning in Drosophila embryos. Cell 1995, 80: 747-756. doi:10.1016/0092-8674(95)90353-4.
55. Wharton RP, Struhl G. RNA regulatory elements mediate control of Drosophila body pattern by the posterior morphogen nanos. Cell 1991, 67:955-967. doi:10.1016/0092-8674(91)90368-9.
56. Curtis D, Treiber D, Tao F, Zamore P, Williamson J, Lehmann R. A CCHC metal-binding domain in Nanos is essential for translational regulation. EMBO J 1997, 16:834-843. doi:10.1093/emboj/16.4.834.
57. Sonoda J, Wharton RP. Recruitment of Nanos to hunchback mRNA by Pumilio. Genes Dev 1999, 13:2704-2712.
58. Sonoda J, Wharton RP. Drosophila Brain Tumor is a translational repressor. Genes Dev 2001, 15:762-773. doi:10.1101/gad.870801.
59. Gamberi C, Peterson DS, He L, Gottlieb E. An anterior function for the Drosophila posterior determinant Pumilio. Development 2002, 129:2699-2710.
60. Asaoka-Taguchi M, Yamada M, Nakamura A, Hanyu K, Kobayashi S. Maternal Pumilio acts together with Nanos in germline development in Drosophila embryos. Nat Cell Biol 1999, 1:431-437. doi:10.1038/15666.
61. Lin H, Spradling AC. A novel group of pumilio mutations affects the asymmetric division of germline stem cells in the Drosophila ovary. Development 1997, 124:2463-2476.
62. Parisi M, Lin H. The Drosophila pumilio gene encodes two functional protein isoforms that play multiple roles in germline development, gonadogenesis, oogenesis and embryogenesis. Genetics 1999, 153:235-250.
63. Forbes A, Lehmann R. Nanos and Pumilio have critical roles in the development and function of Drosophila germline stem cells. Development 1998, 125:679-690.
64. Hodgkin J. Sex determination in the nematode C. elegans: analysis of tra-3 suppressors and characterization of fem genes. Genetics 1986, 15-52.
65. Barton MK, Schedl TB, Kimble J. Gain-of-Function Mutations of fem-3, a Sex-Determination Gene in Caenorhabditis elegans. Genetics 1987, 115:107-119.
66. Ahringer J, Kimble J. Control of the sperm-oocyte switch in Caenorhabditis elegans hermaphrodites by the fem-3 3′ untranslated region. Nature 1991, 349:346-348. doi:10.1038/349346a0.
67. Ahringer J, Rosenquist TA, Lawson DN, Kimble J. The Caenorhabditis elegans sex determining gene fem-3 is regulated post-transcriptionally. EMBO J 1992, 11:2303-2310.
68. Bernstein D, Hook B, Hajarnavis A, Opperman L, Wickens M. Binding specificity and mRNA targets of a C. elegans PUF protein, FBF-1. RNA 2005, 11:447-458. doi:10.1261/rna.7255805.
69. Kraemer B, Crittenden S, Gallegos M, Moulder G, Barstead R, Kimble J, Wickens M. NANOS-3 and FBF proteins physically interact to control the sperm-oocyte switch in Caenorhabditis elegans. Curr Biol 1999, 9:1009-1018. doi:10.1016/S0960-9822(99)80 449-7.
70. Bachorik JL, Kimble J. Redundant control of the Caenorhabditis elegans sperm/oocyte switch by PUF-8 and FBF-1, two distinct PUF RNA-binding proteins. Proc Natl Acad Sci U S A 2005, 102:10893-10897. doi:10.1073/pnas.0504593102.
71. Nakahata S, Kotani T, Mita K, Kawasaki T, Katsu Y, Nagahama Y, Yamashita M. Involvement of Xenopus Pumilio in the translational regulation that is specific to cyclin B1 mRNA during oocyte maturation. Mech Dev 2003, 120:865-880. doi:10.1016/S0925-4773(03)00160-6.
72. Padmanabhan K, Richter JD. Regulated Pumilio-2 binding controls RINGO/Spy mRNA translation and CPEB activation. Genes Dev 2006, 20:199-209. doi:10.1101/gad.1383106.
73. Nadarajan S, Govindan JA, McGovern M, Hubbard EJ, Greenstein D. MSP and GLP-1/Notch signaling coordinately regulate actomyosin-dependent cytoplasmic streaming and oocyte growth in C. elegans. Development 2009, 136:2223-2234. doi:10.1242/dev.034 603.
74. Subramaniam K, Seydoux G. Dedifferentiation of primary spermatocytes into germ cell tumors in C. elegans lacking the pumilio-like protein PUF-8. Curr Biol 2003, 13:134-139. doi:10.1016/S0960-9822(03) 00005-8.
75. Urano J, Fox MS, Reijo Pera RA. Interaction of the conserved meiotic regulators, BOULE (BOL) and PUMILIO-2 (PUM2). Mol Reprod Dev 2005, 71:290-298. doi:10.1002/mrd.20270.
76. Spik A, Oczkowski S, Olszak A, Formanowicz P, Blazewicz J, Jaruzelska J. Human fertility protein PUMILIO2 interacts in vitro with testis mRNA encoding Cdc42 effector 3 (CEP3). Reprod Biol 2006, 6:103-113.
77. Walser CB, Battu G, Hoier EF, Hajnal A. Distinct roles of the Pumilio and FBF translational repressors during C. elegans vulval development. Development 2006, 133:3461-3471. doi:10.1242/dev.02496.
78. Prinz S, Aldridge C, Ramsey SA, Taylor RJ, Galitski T. Control of signaling in a MAP-kinase pathway by an RNA-binding protein. PLoS One 2007, 2:e249. doi:10.1371/journal.pone.0000249.
79. Goldstrohm AC, Hook BA, Seay DJ, Wickens M. PUF proteins bind Pop2p to regulate messenger RNAs. Nat Struct Mol Biol 2006, 13:533-539. doi:10.1038/ nsmb1100.
80. Goldstrohm AC, Seay DJ, Hook BA, Wickens M. PUF protein-mediated deadenylation is catalyzed by Ccr4p. J Biol Chem 2007, 282:109-114. doi:10.1074/jbc. M609413200.
81. Tadauchi T, Matsumoto K, Herskowitz I, Irie K. Post-transcriptional regulation through the HO 3′-UTR by Mpt5, a yeast homolog of Pumilio and FBF. EMBO J 2001, 20:552-561. doi:10.1093/emboj/20.3.552.
82. Hook BA, Goldstrohm AC, Seay DJ, Wickens M. Two yeast PUF proteins negatively regulate a single mRNA. J Biol Chem 2007, 282:15430-15438. doi:10.1074/jbc.M611253200.
83. Kennedy BK, Austriaco NR. Jr, Zhang J, Guarente L. Mutation in the silencing gene SIR4 can delay aging in S. cerevisiae. Cell 1995, 80:485-496. doi:10.1016/00 92-8674(95)90499-9.
84. Kennedy BK, Gotta M, Sinclair DA, Mills K, McNabb DS, Murthy M, Pak SM, Laroche T, Gasser SM, Guarente L. Redistribution of silencing proteins from telomeres to the nucleolus is associated with extension of life span in S. cerevisiae. Cell 1997, 89:381-391. doi:10.1016/S0092-8674(00)80219-6
85. Stewart MS, Krause SA, McGhie J, Gray JV. Mpt5p, a stress tolerance- and lifespan-promoting PUF protein in Saccharomyces cerevisiae, acts upstream of the cell wall integrity pathway. Eukaryot Cell 2007, 6:262-270. doi:10.1128/EC.00188-06.
86. Kaeberlein M, Guarente L. Saccharomyces cerevisiae MPT5 and SSD1 function in parallel pathways to promote cell wall integrity. Genetics 2002, 160:83-95.
87. Olivas W, Parker R. The Puf3 protein is a transcript-specific regulator of mRNA degradation in yeast. EMBO J 2000, 19:6602-6611. doi:10.1093/emboj/ 19.23.6602.
88. Saint-Georges Y, Garcia M, Delaveau T, Jourdren L, Le Crom S, Lemoine S, Tanty V, Devaux F, Jacq C. Yeast mitochondrial biogenesis: a role for the PUF RNA-binding protein Puf3p in mRNA localization. PLoS One 2008, 3:e2293. doi:10.1371/journal. pone.0002293.
89. Eliyahu E, Pnueli L, Melamed D, Scherrer T, Gerber AP, Pines O, Rapaport D, Arava Y. Tom20 mediates localization of mRNAs to mitochondria in a translation-dependent manner. Mol Cell Biol 2010, 30:284-294. doi:MCB.00651-09 [pii]10.1128/MCB. 00651-09.
90. Zipor G, Haim-Vilmovsky L, Gelin-Licht R, Gadir N, Brocard C, Gerst JE. Localization of mRNAs coding for peroxisomal proteins in the yeast, Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 2009, 106:19848-19853. doi:10.1073/pnas.0910754106.
91. Tautz D. Regulation of the Drosophila segmentation gene hunchback by two maternal morphogenetic centres. Nature 1988, 332:281-284. doi:10.1038/3322 81a0.
92. Lamont LB, Crittenden SL, Bernstein D, Wickens M, Kimble J. FBF-1 and FBF-2 regulate the size of the mitotic region in the C. elegans germline. Dev Cell 2004, 7:697-707. doi:10.1016/j.devcel.2004.09.013.
93. Lee MH, Hook B, Pan G, Kershner AM, Merritt C, Seydoux G, Thomson JA, Wickens M, Kimble J. Conserved regulation of MAP kinase expression by PUF RNA-binding proteins. PLoS Genet 2007, 3:e233. doi:10.1371/journal.pgen.0030233.
94. Galgano A, Forrer M, Jaskiewicz L, Kanitz A, Zavolan M, Gerber AP. Comparative analysis of mRNA targets for human PUF-family proteins suggests extensive interaction with the miRNA regulatory system. PLoS One 2008, 3:e3164. doi:10.1371/ journal.pone.0003164.
95. Wickens M, Chritton JJ. Translational repression by PUF proteins in vitro. RNA 2010, 16:1217-1225. doi:10.1261/rna.2070110.
96. Keene JD. RNA regulons: coordination of post-transcriptional events. Nat Rev Genet 2007, 8: 533-543. doi:10.1038/nrg2111.
97. Morris AR, Mukherjee N, Keene JD. Systematic analysis of posttranscriptional gene expression. WIREs Syst Biol Med 2009, 2:162-180. doi:10.1002/wsbm. 54.
98. Gerber AP, Luschnig S, Krasnow MA, Brown PO, Herschlag D. Genome-wide identification of mRNAs associated with the translational regulator PUMILIO in Drosophila melanogaster. Proc Natl Acad Sci U S A 2006, 103:4487-4492. doi:10.1073/pnas.05092 60103.
99. Kershner AM, Kimble J. Genome-wide analysis of mRNA targets for Caenorhabditis elegans FBF, a conserved stem cell regulator. Proc Natl Acad Sci U S A 2010, 107:3936-3941. doi:10.1073/pnas.10004 95107.
100. Zhu D, Stumpf CR, Krahn JM, Wickens M, Hall TM. A 5′ cytosine binding pocket in Puf3p specifies regulation of mitochondrial mRNAs. Proc Natl Acad Sci U S A 2009, 106:20192-20197. doi:10.1073/pnas. 0812079106.
101. Chen G, Li W, Zhang QS, Regulski M, Sinha N, Barditch J, Tully T, Krainer AR, Zhang MQ, Dubnau J. Identification of synaptic targets of Drosophila pumilio. PLoS Comput Biol 2008, 4:e1000026. doi:10.1371/journal.pcbi.1000026.
102. Edwards TA, Pyle SE, Wharton RP, Aggarwal AK. Structure of Pumilio reveals similarity between RNA and peptide binding motifs. Cell 2001, 105:281-289. doi:10.1016/S0092-8674(01)00318-X.
103. Wang X, Zamore PD, Hall TM. Crystal structure of a Pumilio homology domain. Mol Cell 2001, 7: 855-865. doi:10.1016/S1097-2765(01)00229-5.
104. Wang X, McLachlan J, Zamore PD, Hall TM. Modular recognition of RNA by a human pumilio-homology domain. Cell 2002, 110:501-512. doi:10.1016/S00 92-8674(02)00873-5.
105. Cheong CG, Hall TM. Engineering RNA sequence specificity of Pumilio repeats. Proc Natl Acad Sci U S A 2006, 103:13635-13639. doi:10.1073/pnas. 0606294103.
106. Wang Y, Opperman L, Wickens M, Hall TM. Structural basis for specific recognition of multiple mRNA targets by a PUF regulatory protein. Proc Natl Acad Sci U S A 2009, 106:20186-20191. doi:10.1073/pnas. 0812076106.
107. Miller MT, Higgin JJ, Hall TM. Basis of altered RNA-binding specificity by PUF proteins revealed by crystal structures of yeast Puf4p. Nat Struct Mol Biol 2008, 15:397-402. doi:10.1038/nsmb.1390.
108. Stumpf CR, Kimble J, Wickens M. A Caenorhabditis elegans PUF protein family with distinct RNA binding specificity. RNA 2008, 14:1550-1557. doi:10.1261/rna.1095908.
109. Opperman L, Hook B, DeFino M, Bernstein DS, Wickens M. A single spacer nucleotide determines the specificities of two mRNA regulatory proteins. Nat Struct Mol Biol 2005, 12:945-951. doi:10.1038/ nsmb1010.
110. Koh YY, Opperman L, Stumpf C, Mandan A, Keles S, Wickens M. A single C. elegans PUF protein binds RNA in multiple modes. RNA 2009, 15:1090-1099. doi:10.1261/rna.1545309.
111. Gupta YK, Nair DT, Wharton RP, Aggarwal AK. Structures of human Pumilio with noncognate RNAs reveal molecular mechanisms for binding promiscuity. Structure 2008, 16:549-557. doi:10.1016/j.str. 2008.01.006.
112. Gupta YK, Lee TH, Edwards TA, Escalante CR, Kadyrova LY, Wharton RP, Aggarwal AK. Co-occupancy of two Pumilio molecules on a single hunchback NRE. RNA 2009, 15:1029-1035. doi:10.1261/rna. 1327609.
113. Cho PF, Gamberi C, Cho-Park YA, Cho-Park IB, Lasko P, Sonenberg N. Cap-dependent translational inhibition establishes two opposing morphogen gradients in drosophila embryos. Curr Biol 2006, 16:2035-2041. doi:10.1016/j.cub.2006.08.093.
114. Cao Q, Richter JD. Dissolution of the maskin-eIF4E complex by cytoplasmic polyadenylation and poly(A)-binding protein controls cyclin B1 mRNA translation and oocyte maturation. EMBO J 2002, 21:3852-3862. doi:10.1093/emboj/cdf353.
115. Fox M, Urano J, Reijo Pera RA. Identification and characterization of RNA sequences to which human PUMILIO-2 (PUM2) and deleted in Azoospermia-like (DAZL) bind. Genomics 2005, 85:92-105. doi:10.10 16/j.ygeno.2004.10.003.
116. Edwards TA, Wilkinson BD, Wharton RP, Aggarwal AK. Model of the brain tumor-Pumilio translation repressor complex. Genes Dev 2003, 17:2508-2513. doi:10.1101/gad.1119403.
117. Cao Q, Padmanabhan K, Richter JD. Pumilio 2 controls translation by competing with eIF4E for 7-methyl guanosine cap recognition. RNA 2010, 16:221-227. doi:10.1261/rna.1884610.
118. Deng Y, Singer RH, Gu W. Translation of ASH1 mRNA is repressed by Puf6p-Fun12p/eIF5B interaction and released by CK2 phosphorylation. Genes Dev 2008, 22:1037-1050. doi:10.1101/gad.1611308.
119. Muhlrad D, Decker CJ, Parker R. Deadenylation of the unstable mRNA encoded by the yeast MFA2 gene leads to decapping followed by 5′ → 3′ digestion of the transcript. Genes Dev 1994, 8:855-866. doi:10.1101/gad.8.7.855.
120. Lee D, Ohn T, Chiang Y, Quigley G, Yao G, Liu Y, Denis C. PUF3 acceleration of deadenylation in vivo can operate independently of CCR4 activity, possibly involving effects on the PAB1-mRNP structure. J Mol Biol 2010, 562-575. doi:10.1016/j.jmb.2010.04.034.
121. Chritton JJ, Wickens M. Translational repression by PUF proteins in vitro. RNA 2010, 16:1217-1225. doi:rna.2070110[pii]10.1261/rna.2070110.
122. Traven A, Lo T, Lithgow T, Heierhorst J. The yeast PUF protein Puf5 has Pop2-independent roles in response to DNA replication stress. PLoS One 2010, 5:e10651. doi:10.1371/journal.pone.0010651.
123. Fiore R, Khudayberdiev S, Christensen M, Siegel G, Flavell SW, Kim TK, Greenberg ME, Schratt G. Mef2-mediated transcription of the miR379-410 cluster regulates activity-dependent dendritogenesis by fine-tuning Pumilio2 protein levels. EMBO J 2009, 28:697-710. doi:10.1038/emboj.2009.10.
124. Eckmann CR, Kraemer B, Wickens M, Kimble J. GLD-3, a bicaudal-C homolog that inhibits FBF to control germline sex determination in C. elegans. Dev Cell 2002, 3:697-710. doi:10.1016/S1534-5807(02) 00322-2.
125. Kim JY, Lee YC, Kim C. Direct inhibition of Pumilo activity by Bam and Bgcn in Drosophila germ line stem cell differentiation. J Biol Chem 2010, 285: 4741-4746. doi:10.1074/jbc.M109.002014.
126. Foat BC, Houshmandi SS, Olivas WM, Bussemaker HJ. Profiling condition-specific, genome-wide regulation of mRNA stability in yeast. Proc Natl Acad Sci U S A 2005, 102:17675-17680. doi:10.1073/pnas. 0503803102.
127. Souza GM, da Silva AM, Kuspa A. Starvation promotes Dictyostelium development by relieving PufA inhibition of PKA translation through the YakA kinase pathway. Development 1999, 126:3263-3274.