Abstract
The Pumilio (Pum)/Puf family proteins are ubiquitously present across eukaryotes, including yeast, plants and humans. They generally bind to the 3′ untranslated regions of single stranded RNA targets in a sequence specific manner and destabilize them, although a few reports suggest their role in stabilizing the target transcripts. The Pum isoforms are implicated in a wide array of biological processes including stem cell maintenance, development, ribosome biogenesis as well as human diseases. Further studies on Pum would be interesting and important to understand their evolutionarily conserved and divergent features across species, which can have potential implications in medicine, plant sciences as well as basic molecular and cell biological studies. A large number of research reports exists, pertaining to various aspects of Pum, in individual experimental systems. This review is a comprehensive summary of the functions, types, mechanism of action as well as the regulation of Pum in various species. Also, the research questions to be addressed in future are discussed.
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References
Glisovic T, Bachorik JL, Yong J, Dreyfuss G (2008) RNA-binding proteins and posttranscriptional gene regulation. FEBS Lett 582(14):1977–1986. https://doi.org/10.1016/j.febslet.2008.03.004
Van Kouwenhove M, Kedde M, Agami R (2011) MicroRNA regulation by RNAbinding proteins and its implications for cancer. Nat Rev Cancer 11(9):644. https://doi.org/10.1038/nrc3107
Lu G, Hall TM (2011) Alternate modes of cognate RNA recognition by human PUMILIO proteins. Structure 19(3):361–367. https://doi.org/10.1016/j.str.2010.12.019
Francischini CW, Quaggio RB (2009) Molecular characterization of Arabidopsis thaliana PUF proteins–binding specificity and target candidates. FEBS J 276(19):545670. https://doi.org/10.1111/j.1742-4658.2009.07230.x
Ryder SP (2011) Pumilio RNA recognition: the consequence of promiscuity. Structure 19(3):277–279. https://doi.org/10.1016/j.str.2011.02.006
Macdonald PM (1992) The Drosophila pumilio gene: an unusually long transcription unit and an unusual protein. Development 114(1):221–232
Murata Y, Wharton RP (1995) Binding of pumilio to maternal hunchback mRNA is required for posterior patterning in Drosophila embryos. Cell 80(5):747–756. https://doi.org/10.1016/0092-8674(95)90353-4
Zhang B, Gallegos M, Puoti A, Durkin E, Fields S, Kimble J, Wickens MP (1997) A conserved RNA-binding protein that regulates sexual fates in the C. elegans hermaphrodite germ line. Nature 390(6659):477. https://doi.org/10.1038/37297
Wang X, Zamore PD, Hall TM (2001) Crystal structure of a Pumilio homology domain. Mol Cell 7(4):855–865
Spassov D, Jurecic R (2003) The PUF family of RNA-binding proteins: does evolutionarily conserved structure equal conserved function? IUBMB Life 55(7):359–366. https://doi.org/10.1080/15216540310001603093
Qiu C, McCann KL, Wine RN, Baserga SJ, Hall TM (2014) A divergent Pumilio repeat protein family for pre-rRNA processing and mRNA localization. Proc Natl Acad Sci USA 111(52):18554–18559. https://doi.org/10.1073/pnas.1407634112
Zhang J, McCann KL, Qiu C, Gonzalez LE, Baserga SJ, Hall TM (2016) Nop9 is a PUF-like protein that prevents premature cleavage to correctly process pre-18S rRNA. Nat Commun 7:13085. https://doi.org/10.1038/ncomms13085
Zhang C, Muench DG (2015) A nucleolar PUF RNA-binding protein with specificity for a unique RNA sequence. J Biol Chem 290(50):3010818. https://doi.org/10.1074/jbc.M115.691675
Van Etten J, Schagat TL, Hrit J, Weidmann CA, Brumbaugh J, Coon JJ, Goldstrohm AC (2012) Human Pumilio proteins recruit multiple deadenylases to efficiently repress messenger RNAs. J Biol Chem 287(43):36370–36383. https://doi.org/10.1074/jbc.M112.373522.15
Gu W, Deng Y, Zenklusen D, Singer RH (2004) A new yeast PUF family protein, Puf6p, represses ASH1 mRNA translation and is required for its localization. Genes Dev 18(12):1452–1465. https://doi.org/10.1101/gad.1189004
Miller MA, Olivas WM (2011) Roles of Puf proteins in mRNA degradation and translation. Wiley Interdiscip Rev RNA 2(4):471–492. https://doi.org/10.1002/wrna.69
Archer SK, Luu VD, de Queiroz RA, Brems S, Clayton C (2009) Trypanosoma brucei PUF9 regulates mRNAs for proteins involved in replicative processes over the cell cycle. PLoS Pathog 5(8):e1000565. https://doi.org/10.1371/journal.ppat.1000565
Kaye JA, Rose NC, Goldsworthy B, Goga A, Noelle DL (2009) A 3′ UTR pumiliobinding element directs translational activation in olfactory sensory neurons. Neuron 61(1):57–70. https://doi.org/10.1016/j.neuron.2008.11.012
Naudin C, Hattabi A, Michelet F, Miri-Nezhad A, Benyoucef A, Pflumio F, Guillonneau F, Fichelson S, Vigon I, Dusanter-Fourt I, Lauret E (2017) PUMILIO/FOXP1 signaling drives expansion of hematopoietic stem/progenitor and leukemia cells. Blood 129(18):2493–2506. https://doi.org/10.1182/blood-2016-10-747436
Walser CB, Battu G, Hoier EF, Hajnal A (2006) Distinct roles of the Pumilio and FBF translational repressors during C. elegans vulval development. Development 133(17):3461–3471. https://doi.org/10.1242/dev.02496
Caro F, Bercovich N, Atorrasagasti C, Levin MJ, Vázquez MP (2006) Trypanosoma cruzi: analysis of the complete PUF RNA-binding protein family. Exp Parasitol 113(2):112–124. https://doi.org/10.1016/j.exppara.2005.12.015
Cui L, Fan Q, Li J (2002) The malaria parasite Plasmodium falciparum encodes members of the Puf RNA-binding protein family with conserved RNA binding activity. Nucleic Acids Res 30(21):4607–4617. https://doi.org/10.1093/nar/gkf600
Kurisaki I, Iwai T, Yamashita M, Kobayashi M, Ito E, Matsuoka I (2007) Identification and expression analysis of rainbow trout pumilio-1 and pumilio-2. Cell Tissue Res 327(1):33–42. https://doi.org/10.1007/s00441-006-0260-y
Lee JY, Lim JM, Kim DK, Zheng YH, Moon S, Han BK, Song KD, Kim H, Han JY (2008) Identification and gene expression profiling of the Pum1 and Pum2 members of the Pumilio family in the chicken. Mol Reprod Dev 75(1):184–190. https://doi.org/10.1002/mrd.20765
Liu M, Miao J, Liu T, Sullivan WJ, Cui L, Chen X (2014) Characterization of TgPuf1, a member of the Puf family RNA-binding proteins from Toxoplasma gondii. Parasit Vectors 7(1):141. https://doi.org/10.1186/1756-3305-7-141
Spassov DS, Jurecic R (2002) Cloning and comparative sequence analysis of PUM1 and PUM2 genes, human members of the Pumilio family of RNA-binding proteins. Gene 299(1–2):195–204. https://doi.org/10.1016/s0378-1119(02)01060-0
Tam PP, Barrette-Ng IH, Simon DM, Tam MW, Ang AL, Muench DG (2010) The Puf family of RNA-binding proteins in plants: phylogeny, structural modeling, activity and subcellular localization. BMC Plant Biol 10(1):44. https://doi.org/10.1186/1471-2229-10-44
Chen G, Li W, Zhang QS, Regulski M, Sinha N, Barditch J, Tully T, Krainer AR, Zhang MQ, Dubnau J (2008) Identification of synaptic targets of Drosophila pumilio. PLoS Comput Biol 4(2):e1000026. https://doi.org/10.1371/journal.pcbi.1000026
Muraro NI, Weston AJ, Gerber AP, Luschnig S, Moffat KG, Baines RA (2008) Pumilio binds para mRNA and requires Nanos and Brat to regulate sodium current in Drosophila motoneurons. J Neurosci 28(9):2099–2109. https://doi.org/10.1523/JNEUROSCI.5092-07.2008
Menon KP, Sanyal S, Habara Y, Sanchez R, Wharton RP, Ramaswami M, Zinn K (2004) The translational repressor Pumilio regulates presynaptic morphology and controls postsynaptic accumulation of translation factor eIF-4E. Neuron 44(4):663–676. https://doi.org/10.1016/j.neuron.2004.10.028
Ye B, Petritsch C, Clark IE, Gavis ER, Jan LY, Jan YN (2004) Nanos and Pumilio are essential for dendrite morphogenesis in Drosophila peripheral neurons. Curr Biol 14(4):314–321. https://doi.org/10.1016/j.cub.2004.01.052
Vessey JP, Schoderboeck L, Gingl E, Luzi E, Riefler J, Di Leva F, Karra D, Thomas S, Kiebler MA, Macchi P (2010) Mammalian Pumilio 2 regulates dendrite morphogenesis and synaptic function. Proc Natl Acad Sci USA 107(7):3222–3227. https://doi.org/10.1073/pnas.0907128107
Driscoll HE, Muraro NI, He M, Baines RA (2013) Pumilio-2 regulates translation of Nav1. 6 to mediate homeostasis of membrane excitability. J Neurosci 33(23):9644–9654. https://doi.org/10.1523/JNEUROSCI.0921-13.2013
Siemen H, Colas D, Heller HC, Brüstle O, Pera RAR (2011) Pumilio-2 function in the mouse nervous system. PLoS ONE 6(10):e25932. https://doi.org/10.1371/journal.pone.0025932
Forbes A, Lehmann R (1998) Nanos and Pumilio have critical roles in the development and function of Drosophila germline stem cells. Development 125(4):679–690
Parisi M, Lin H (1999) The Drosophila pumilio gene encodes two functional protein isoforms that play multiple roles in germline development, gonadogenesis, oogenesis and embryogenesis. Genetics 153(1):235–250
Crittenden SL, Bernstein DS, Bachorik JL, Thompson BE, Gallegos M, Petcherski AG, Moulder G, Barstead R, Wickens M, Kimble J (2002) A conserved RNA-binding protein controls germline stem cells in Caenorhabditis elegans. Nature 417(6889):660. https://doi.org/10.1038/nature754
Miao J, Li J, Fan Q, Li X, Li X, Cui L (2010) The Puf-family RNA-binding protein PfPuf2 regulates sexual development and sex differentiation in the malaria parasite Plasmodium falciparum. J Cell Sci 123(7):1039–1049
Salvetti A, Rossi L, Lena A, Batistoni R, Deri P, Rainaldi G, Locci MT, Evangelista M, Gremigni V (2005) DjPum, a homologue of Drosophila Pumilio, is essential to planarian stem cell maintenance. Development 132(8):1863–1874. https://doi.org/10.1242/dev.01785
Kuo MW, Wang SH, Chang JC, Chang CH, Huang LJ, Lin HH, Yu AL, Li WH, Yu J (2009) A novel puf-A gene predicted from evolutionary analysis is involved in the development of eyes and primordial germ-cells. PLoS ONE 4(3):e4980. https://doi.org/10.1371/journal.pone.0004980
Amaral DG, Scharfman HE, Lavenex P (2007) The dentate gyrus: fundamental neuroanatomical organization (dentate gyrus for dummies). Prog Brain Res 163:3–790. https://doi.org/10.1016/S0079-6123(07)63001-5
Zhang M, Chen D, Xia J, Han W, Cui X, Neuenkirchen N, Hermes G, Sestan N, Lin H (2017) Post-transcriptional regulation of mouse neurogenesis by Pumilio proteins. Genes Dev 31(13):1354–1369. https://doi.org/10.1101/gad.298752.117
Lin K, Zhang S, Shi Q, Zhu M, Gao L, Xia W, Geng B, Zheng Z, Xu EY (2018) Essential requirement of mammalian Pumilio family in embryonic development. Mol Biol Cell 29(24):2922–2932. https://doi.org/10.1091/mbc.E18-06-0369
Moore FL, Jaruzelska J, Fox MS, Urano J, Firpo MT, Turek PJ, Dorfman DM, Pera RA (2003) 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 USA 100(2):538–543. https://doi.org/10.1073/pnas.0234478100
Shigunov P, Sotelo-Silveira J, Kuligovski C, de Aguiar AM, Rebelatto CK, Moutinho JA, Brofman PS, Krieger MA, Goldenberg S, Munroe D, Correa A (2011) PUMILIO-2 is involved in the positive regulation of cellular proliferation in human adipose-derived stem cells. Stem Cells Dev 21(2):217–227. https://doi.org/10.1089/scd.2011.0143
Aggarwal P, Yadav RK, Reddy GV (2010) Identification of novel markers for stemcell niche of Arabidopsis shoot apex. Gene Expr Patterns 10(6):259–264. https://doi.org/10.1016/j.gep.2010.05.004
Shanmugam T, Abbasi N, Kim HS, Kim HB, Park NI, Park GT, Oh SA, Park SK, Muench DG, Choi Y, Park YI (2017) An Arabidopsis divergent pumilio protein, APUM 24, is essential for embryogenesis and required for faithful pre-rRNA processing. Plant J 92(6):1092–1105. https://doi.org/10.1111/tpj.13745
Somssich M, Je BI, Simon R, Jackson D (2016) CLAVATA-WUSCHEL signaling in the shoot meristem. Development 143(18):3238–3248. https://doi.org/10.1242/dev.133645
Lynn K, Fernandez A, Aida M, Sedbrook J, Tasaka M, Masson P, Barton MK (1999) The PINHEAD/ZWILLE gene acts pleiotropically in Arabidopsis development and has overlapping functions with the ARGONAUTE1 gene. Development 126(3):469–481
Bhalla PL, Singh MB (2006) Molecular control of stem cell maintenance in shoot apical meristem. Plant Cell Rep 25(4):249–256. https://doi.org/10.1007/s00299-005-0071-8
Wang Z, Sun X, Wee J, Guo X, Gu Z (2019) Novel insights into global translational regulation through Pumilio family RNA-binding protein Puf3p revealed by ribosomal profiling. Curr Genet 65(1):201–212. https://doi.org/10.1007/s00294-018-0862-4
Liang X, Hart KJ, Dong G, Siddiqui FA, Sebastian A, Li X, Albert I, Miao J, Lindner SE, Cui L (2018) Puf3 participates in ribosomal biogenesis in malaria parasites. J Cell Sci 131(6):jcs212597. https://doi.org/10.1242/jcs.212597
Droll D, Archer S, Fenn K, Delhi P, Matthews K, Clayton C (2010) The trypanosome Pumilio-domain protein PUF7 associates with a nuclear cyclophilin and is involved in ribosomal RNA maturation. FEBS Lett 584(6):1156–1162. https://doi.org/10.1016/j.febslet.2010.02.018
Yu J, Cho HC, Huang Y, Hung JT, Lai LC, Wang SH, Liu YH, Cho IM, Kuo MW, Cheng PY, Ho MY (2018) Human Puf-A, a novel component of 90S pre-ribosome, links ribosome biogenesis to cancer progression. bioRxiv. https://doi.org/10.1101/281857v1.abstract
Abbasi N, Kim HB, Park NI, Kim HS, Kim YK, Park YI, Choi SB (2010) APUM23, a nucleolar Puf domain protein, is involved in pre-ribosomal RNA processing and normal growth patterning in Arabidopsis. Plant J 64(6):960–976. https://doi.org/10.1111/j.1365313X.2010.04393.x
Maekawa S, Ishida T, Yanagisawa S (2018) Reduced expression of APUM24, encoding a novel rRNA processing factor, induces sugar-dependent nucleolar stress and altered sugar responses in Arabidopsis thaliana. Plant Cell 30(1):209–227
Hotz M, Nelson WJ (2017) Pumilio-dependent localization of mRNAs at the cell front coordinates multiple pathways required for chemotaxis. Nat Commun 8(1):1366. https://doi.org/10.1038/s41467-017-01536-x
Lin K, Qiang W, Zhu M, Ding Y, Shi Q, Chen X, Zsiros E, Wang K, Yang X, Kurita T, Xu EY (2019) Mammalian Pum1 and Pum2 control body size via translational regulation of the cell cycle inhibitor Cdkn1b. Cell Rep 26(9):2434–2450. https://doi.org/10.1016/j.celrep.2019.01.111
Brocard M, Khasnis S, Wood CD, Shannon-Lowe C, West MJ (2018) Pumilio directs deadenylation-associated translational repression of the cyclin-dependent kinase 1 activator RGC-32. Nucleic Acids Res 46(7):3707–3725. https://doi.org/10.1093/nar/gky038
Miles WO, Tschöp K, Herr A, Ji JY, Dyson NJ (2012) Pumilio facilitates miRNA regulation of the E2F3 oncogene. Genes Dev 26(4):356–368. https://doi.org/10.1101/gad.182568.111
Liu Y, Qu L, Liu Y, Roizman B, Zhou GG (2017) PUM1 is a biphasic negative regulator of innate immunity genes by suppressing LGP2. Proc Natl Acad Sci USA 114(33):E6902–E6911. https://doi.org/10.1073/pnas.1708713114
Bohn JA, Van Etten JL, Schagat TL, Bowman BM, McEachin RC, Freddolino PL, Goldstrohm AC (2017) Identification of diverse target RNAs that are functionally regulated by human Pumilio proteins. Nucleic Acids Res 46(1):362–386. https://doi.org/10.1093/nar/gkx1120
D’Amico D, Mottis A, Potenza F, Sorrentino V, Li H, Romani M, Lemos V, Schoonjans K, Zamboni N, Knott G, Schneider BL (2019) The RNA-binding protein PUM2 impairs mitochondrial dynamics and mitophagy during aging. Mol Cell 73(4):775–787
Yamada T, Imamachi N, Imamura K, Kawamura T, Suzuki Y, Nagahama M, Akimitsu N (2019) Systematic analysis of targets of Pumilio (PUM)-mediated mRNA decay identifies a role of PUM1 in regulating DNA damage response pathway. bioRxiv. https://doi.org/10.1101/387381
Elguindy MM, Kopp F, Goodarzi M, Rehfeld F, Thomas A, Chang TC, Mendell JT (2019) PUMILIO, but not RBMX, binding is required for regulation of genomic stability by noncoding RNA NORAD. bioRxiv. https://doi.org/10.1101/645960v1.abstract
Huang KC, Lin WC, Cheng WH (2018) Salt hypersensitive mutant 9, a nucleolar APUM23 protein, is essential for salt sensitivity in association with the ABA signaling pathway in Arabidopsis. BMC Plant Biol 8(1):40. https://doi.org/10.1186/s12870-018-1255-z
Huh SU, Kim MJ, Paek KH (2013) Arabidopsis Pumilio protein APUM5 suppresses Cucumber mosaic virus infection via direct binding of viral RNAs. Proc Natl Acad Sci USA 110(2):779–784. https://doi.org/10.1073/pnas.1214287110
Huh SU, Paek KH (2014) APUM5, encoding a Pumilio RNA binding protein, negatively regulates abiotic stress responsive gene expression. BMC Plant Biol 14(1):75. https://doi.org/10.1186/1471-2229-14-75
Xiang Y, Nakabayashi K, Ding J, He F, Bentsink L, Soppe WJ (2014) Reduced Dormancy5 encodes a protein phosphatase 2C that is required for seed dormancy in Arabidopsis. Plant Cell 26(11):4362–4375. https://doi.org/10.1105/tpc.114.132811
Nyikó T, Auber A, Bucher E (2019) Functional and molecular characterization of the conserved Arabidopsis PUMILIO protein, APUM9. Plant Mol Biol 100(1–2):199–214. https://doi.org/10.1007/s11103-019-00853-7
Dai H, Shen K, Yang Y, Su X, Luo Y, Jiang Y, Shuai L, Zheng P, Chen Z, Bie P (2019) PUM1 knockdown prevents tumor progression by activating the PERK/eIF2/ATF4 signaling pathway in pancreatic adenocarcinoma cells. Cell Death Dis 10(8):1–5
Guan X, Chen S, Liu Y, Wang LL, Zhao Y, Zong ZH (2018) PUM1 promotes ovarian cancer proliferation, migration and invasion. Biochem Biophys Res Commun 497(1):313–318
Miles WO, Lembo A, Volorio A, Brachtel E, Tian B, Sgroi D, Provero P, Dyson N (2016) Alternative polyadenylation in triple-negative breast tumors allows NRAS and c-JUN to bypass PUMILIO posttranscriptional regulation. Cancer Res 76(24):7231–7241
Follwaczny P, Schieweck R, Riedemann T, Demleitner A, Straub T, Klemm AH, Bilban M, Sutor B, Popper B, Kiebler MA (2017) Pumilio2-deficient mice show a predisposition for epilepsy. Dis Models Mech 10(11):1333–1342
Lin WH, Giachello CN, Baines RA (2017) Seizure control through genetic and pharmacological manipulation of Pumilio in Drosophila: a key component of neuronal homeostasis. Dis Models Mech 10(2):141–150
Gennarino VA, Singh RK, White JJ, De Maio A, Han K, Kim JY, Jafar-Nejad P, Di Ronza A, Kang H, Sayegh LS, Cooper TA (2015) Pumilio1 haploinsufficiency leads to SCA1-like neurodegeneration by increasing wild-type Ataxin1 levels. Cell 160(6):1087–1098
Gennarino VA, Palmer EE, McDonell LM, Wang L, Adamski CJ, Koire A, See L, Chen CA, Schaaf CP, Rosenfeld JA, Panzer JA (2018) A mild PUM1 mutation is associated with adult-onset ataxia, whereas haploinsufficiency causes developmental delay and seizures. Cell 172(5):924–936
Edwards TA, Pyle SE, Wharton RP, Aggarwal AK (2001) Structure of Pumilio reveals similarity between RNA and peptide binding motifs. Cell 105(2):281–289. https://doi.org/10.1016/s0092-8674(01)00318-x
Wang X, McLachlan J, Zamore PD, Hall TM (2002) Modular recognition of RNA by a human pumilio-homology domain. Cell 110(4):501–512. https://doi.org/10.1016/s00928674(02)00873-5
Gupta YK, Nair DT, Wharton RP, Aggarwal AK (2008) Structures of human Pumilio with noncognate RNAs reveal molecular mechanisms for binding promiscuity. Structure 16(4):549–557. https://doi.org/10.1016/j.str.2008.01.006
Bernstein D, Hook B, Hajarnavis A, Opperman L, Wickens M (2005) Binding specificity and mRNA targets of a C. elegans PUF protein, FBF-1. RNA 11(4):447–458. https://doi.org/10.1261/rna.7255805
Sajek M, Janecki DM, Smialek MJ, Ginter-Matuszewska B, Spik A, Oczkowski S, Ilaslan E, Kusz-Zamelczyk K, Kotecki M, Blazewicz J, Jaruzelska J (2019) PUM1 and PUM2 exhibit different modes of regulation for SIAH1 that involve cooperativity with NANOS paralogues. Cell Mol Life Sci 76(1):147–161. https://doi.org/10.1007/s00018-018-2926-5
Vaidyanathan PP, AlSadhan I, Merriman DK, Al-Hashimi HM, Herschlag D (2017) Pseudouridine and N6-methyladenosine modifications weaken PUF protein/RNA interactions. RNA 23(5):611–618. https://doi.org/10.1261/rna.060053.116
Houshmandi SS, Olivas WM (2005) Yeast Puf3 mutants reveal the complexity of Puf-RNA binding and identify a loop required for regulation of mRNA decay. RNA 11(11):1655–1666. https://doi.org/10.1261/rna.2168505
Malik S, Jang W, Park SY, Kim JY, Kwon KS, Kim C (2019) The target specificity of the RNA binding protein Pumilio is determined by distinct co-factors. Biosci Rep 39(6):BSR20190099
Qiu C, Dutcher RC, Porter DF, Arava Y, Wickens M, Hall TM (2019) Distinct RNA-binding modules in a single PUF protein cooperate to determine RNA specificity. Nucleic Acids Res 47(16):8770–8784
Zhao J, Hyman L, Moore C (1999) Formation of mRNA 3′ ends in eukaryotes: mechanism, regulation, and interrelationships with other steps in mRNA synthesis. Microbiol Mol Biol Rev 63(2):405–445
Gorgoni B, Gray NK (2004) The roles of cytoplasmic poly (A)-binding proteins in regulating gene expression: a developmental perspective. Brief Funct Genom Proteomic 3(2):125–141. https://doi.org/10.1093/bfgp/3.2.125
Goldstrohm AC, Wickens M (2008) Multifunctional deadenylase complexes diversify mRNA control. Nat Rev Mol Cell Biol 9(4):337–344. https://doi.org/10.1038/nrm2370
Inada T, Makino S (2014) Novel roles of the multi-functional CCR90-NOT complex in posttranscriptional regulation. Front Genet 5:135. https://doi.org/10.3389/fgene.2014.00135
Arae T, Morita K, Imahori R, Suzuki Y, Yasuda S, Sato T, Yamaguchi J, Chiba Y (2019) Identification of Arabidopsis CCR91-NOT complexes with Pumilio RNA-Binding Proteins, APUM5 and APUM2. Plant Cell Physiol. https://doi.org/10.1093/pcp/pcz089
Goldstrohm AC, Hook BA, Seay DJ, Wickens M (2006) PUF proteins bind Pop2p to regulate messenger RNAs. Nat Struct Mol Biol 13(6):533. https://doi.org/10.1038/nsmb1100
Joly W, Chartier A, Rojas-Rios P, Busseau I, Simonelig M (2013) The CCR93 deadenylase acts with Nanos and Pumilio in the fine-tuning of Mei-P26 expression to promote germline stem cell self-renewal. Stem Cell Rep 1(5):411–424. https://doi.org/10.1016/j.stemcr.2013.09.007
Webster MW, Stowell JA, Passmore LA (2019) RNA-binding proteins distinguish between similar sequence motifs to promote targeted deadenylation by Ccr4-Not. Elife 8:e40670. https://doi.org/10.7554/eLife.40670
Richter JD, Sonenberg N (2005) Regulation of cap-dependent translation by eIF4E inhibitory proteins. Nature 433(7025):477. https://doi.org/10.1038/nature03205
Gallie DR (1998) A tale of two termini: a functional interaction between the termini of an mRNA is a prerequisite for efficient translation initiation. Gene 216(1):11
Hodgman R, Tay J, Mendez R, Richter JD (2001) CPEB phosphorylation and cytoplasmic polyadenylation are catalyzed by the kinase IAK1/Eg2 in maturing mouse oocytes. Development 128(14):2815–2822
Campbell ZT, Menichelli E, Friend K, Wu J, Kimble J, Williamson JR, Wickens M (2012) Identification of a conserved interface between PUF and CPEB proteins. J Biol Chem 287(22):18854–18862. https://doi.org/10.1074/jbc.M112.352815
Ivshina M, Lasko P, Richter JD (2014) Cytoplasmic polyadenylation element binding proteins in development, health, and disease. Annu Rev Cell Dev Biol 30:393–415. https://doi.org/10.1146/annurev-cellbio-101011-155831
Cao Q, Padmanabhan K, Richter JD (2010) Pumilio 2 controls translation by competing with eIF4E for 7-methyl guanosine cap recognition. RNA 16(1):221–227. https://doi.org/10.1261/rna.1884610
Chritton JJ, Wickens M (2011) A role for the poly (A)-binding protein Pab1p in PUF protein mediated repression. J Biol Chem 286(38):33268–33278. https://doi.org/10.1074/jbc.M111.264572
Sonoda J, Wharton RP (2001) Drosophila brain tumor is a translational repressor. Genes Dev 15(6):762–773. https://doi.org/10.1101/gad.870801
Weidmann CA, Qiu C, Arvola RM, Lou TF, Killingsworth J, Campbell ZT, Hall TM, Goldstrohm AC (2016) Drosophila Nanos acts as a molecular clamp that modulates the RNA binding and repression activities of Pumilio. Elife 5:e17096. https://doi.org/10.7554/eLife.17096
Cho PF, Gamberi C, Cho-Park YA, Cho-Park IB, Lasko P, Sonenberg N (2006) Cap dependent translational inhibition establishes two opposing morphogen gradients in Drosophila embryos. Curr Biol 16(20):2035–2041. https://doi.org/10.1016/j.cub.2006.08.093
Weidmann CA, Goldstrohm AC (2012) Drosophila Pumilio protein contains multiple autonomous repression domains that regulate mRNAs independently of Nanos and brain tumor. Mol Cell Biol 32(2):527–540. https://doi.org/10.1128/MCB.06052-11
Kedde M, Van Kouwenhove M, Zwart W, Vrielink JA, Elkon R, Agami R (2010) A Pumilio induced RNA structure switch in p27-3′ UTR controls miR-221 and miR-222 accessibility. Nat Cell Biol 12(10):1014. https://doi.org/10.1038/ncb2105
Lin WH, Baines RA (2019) Myocyte enhancer factor-2 and p300 interact to regulate the expression of homeostatic regulator Pumilio in Drosophila. Eur J Neurosci 50(1):1727–1740. https://doi.org/10.1111/ejn.14357
Fiore R, Khudayberdiev S, Christensen M, Siegel G, Flavell SW, Kim TK, Greenberg ME, Schratt G (2009) Mef2-mediated transcription of the miR379–410 cluster regulates activity-dependent dendritogenesis by fine-tuning Pumilio2 protein levels. EMBO J 28(6):697–710. https://doi.org/10.1038/emboj.2009.10
Lin WH, He M, Fan YN, Baines RA (2018) An RNAi-mediated screen identifies novel targets for next-generation antiepileptic drugs based on increased expression of the homeostatic regulator pumilio. J Neurogenet 32(2):106–117. https://doi.org/10.1080/01677063.2018.1465570
Carreira-Rosario A, Bhargava V, Hillebrand J, Kollipara RK, Ramaswami M, Buszczak M (2016) Repression of Pumilio protein expression by Rbfox1 promotes germ cell differentiation. Dev Cell 36(5):562–571. https://doi.org/10.1016/j.devcel.2016.02.010
Lee S, Kopp F, Chang TC, Sataluri A, Chen B, Sivakumar S, Yu H, Xie Y, Mendell JT (2016) Noncoding RNA NORAD regulates genomic stability by sequestering PUMILIO proteins. Cell 164(1–2):69–80. https://doi.org/10.1016/j.cell.2015.12.017
Kopp F, Elguindy MM, Yalvac ME, Zhang H, Chen B, Gillett FA, Lee S, Sivakumar S, Yu H, Xie Y, Mishra P (2019) PUMILIO hyperactivity drives premature aging of Norad deficient mice. Elife 8:e42650. https://doi.org/10.7554/eLife.42650
Lee CD, Tu BP (2015) Glucose-regulated phosphorylation of the PUF protein Puf3 regulates the translational fate of its bound mRNAs and association with RNA granules. Cell Rep 11(10):1638–1650. https://doi.org/10.1016/j.celrep.2015.05.014
Zoncu R, Efeyan A, Sabatini DM (2011) mTOR: from growth signal integration to cancer, diabetes and ageing. Nat Rev Mol Cell Biol 12(1):21. https://doi.org/10.1038/nrm3025
Tichon A, Perry RB, Stojic L, Ulitsky I (2018) SAM68 is required for regulation of Pumilio by the NORAD long noncoding RNA. Genes Dev 32(1):70–78. https://doi.org/10.1101/gad.309138.117
Gamberi C, Peterson DS, He L, Gottlieb E (2002) An anterior function for the Drosophila posterior determinant Pumilio. Development 129(11):2699–2710
Mee CJ, Pym EC, Moffat KG, Baines RA (2004) Regulation of neuronal excitability through pumilio-dependent control of a sodium channel gene. J Neurosci 24(40):8695–8703. https://doi.org/10.1523/JNEUROSCI.2282-04.2004
Menon KP, Andrews S, Murthy M, Gavis ER, Zinn K (2009) The translational repressors Nanos and Pumilio have divergent effects on presynaptic terminal growth and postsynaptic glutamate receptor subunit composition. J Neurosci 29(17):5558–5572. https://doi.org/10.1523/JNEUROSCI.0520-09.2009
Wreden C, Verrotti AC, Schisa JA, Lieberfarb ME, Strickland S (1997) Nanos and pumilio establish embryonic polarity in Drosophila by promoting posterior deadenylation of hunchback mRNA. Development 124(15):3015–3023
Lublin AL, Evans TC (2007) The RNA-binding proteins PUF-5, PUF-6, and PUF-7 reveal multiple systems for maternal mRNA regulation during C. elegans oogenesis. Dev Biol 303(2):635–649. https://doi.org/10.1016/j.ydbio.2006.12.004
Nolde MJ, Saka N, Reinert KL, Slack FJ (2007) 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 305(2):551–563
Tadauchi T, Matsumoto K, Herskowitz I, Irie K (2001) Post-transcriptional regulation through the HO 3′-UTR by Mpt5, a yeast homolog of Pumilio and FBF. EMBO J 20(3):552–561. https://doi.org/10.1093/emboj/20.3.552
Haramati O, Brodov A, Yelin I, Atir-Lande A, Samra N, Arava Y (2017) Identification and characterization of roles for Puf1 and Puf2 proteins in the yeast response to high calcium. Sci Rep 7(1):3037. https://doi.org/10.1038/s41598-017-02873-z
Glerum DM, Shtanko A, Tzagoloff A (1996) Characterization of COX17, a yeast gene involved in copper metabolism and assembly of cytochrome oxidase. J Biol Chem 271(24):14504–14509. https://doi.org/10.1074/jbc.271.24.14504
Jackson JS, Houshmandi SS, Leban FL, Olivas WM (2004) Recruitment of the Puf3 protein to its mRNA target for regulation of mRNA decay in yeast. RNA 10(10):162536. https://doi.org/10.1261/rna.7270204
Dallagiovanna B, Correa A, Probst CM, Holetz F, Smircich P, de Aguiar AM, Mansur F, da Silva CV, Mortara RA, Garat B, Buck GA (2008) Functional genomic characterization of mRNAs associated with TcPUF6, a pumilio-like protein from Trypanosoma cruzi. J Biol Chem 283(13):8266–8273. https://doi.org/10.1074/jbc.M703097200
Nakahata S, Kotani T, Mita K, Kawasaki T, Katsu Y, Nagahama Y, Yamashita M (2003) Involvement of Xenopus Pumilio in the translational regulation that is specific to cyclin B1 mRNA during oocyte maturation. Mech Dev 120(8):865–880
Padmanabhan K, Richter JD (2006) Regulated Pumilio-2 binding controls RINGO/Spy mRNA translation and CPEB activation. Genes Dev 20(2):199–209. https://doi.org/10.1101/gad.1383106
Acknowledgements
The research in the authors’ lab was funded by grants to BS, from Department of Science and Technology, Govt. of India (Grant Sanction Number: SB/YS/LS-188/2014) and Department of Biotechnology, Govt. of India (Grant Sanction Number: BT/Bio-CARe/02/10,078/2013–14). MJN receives and acknowledges the DST-INSPIRE Fellowship (IF170376) from Department of Science and Technology, Govt. of India. The authors are thankful to Mr. S A Sheshadri for critical reading and suggestions regarding the manuscript. The authors thank SASTRA Deemed to be University for the infrastructural facilities.
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Nishanth, M.J., Simon, B. Functions, mechanisms and regulation of Pumilio/Puf family RNA binding proteins: a comprehensive review. Mol Biol Rep 47, 785–807 (2020). https://doi.org/10.1007/s11033-019-05142-6
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DOI: https://doi.org/10.1007/s11033-019-05142-6