3q0r Citations

Alternate modes of cognate RNA recognition by human PUMILIO proteins.

Structure 19 361-7 (2011)
Related entries: 3q0l, 3q0m, 3q0n, 3q0o, 3q0p, 3q0q, 3q0s

Cited: 38 times
EuropePMC logo PMID: 21397187

Abstract

Human PUMILIO1 (PUM1) and PUMILIO2 (PUM2) are members of the PUMILIO/FBF (PUF) family that regulate specific target mRNAs posttranscriptionally. Recent studies have identified mRNA targets associated with human PUM1 and PUM2. Here, we explore the structural basis of natural target RNA recognition by human PUF proteins through crystal structures of the RNA-binding domains of PUM1 and PUM2 in complex with four cognate RNA sequences, including sequences from p38α and erk2 MAP kinase mRNAs. We observe three distinct modes of RNA binding around the fifth RNA base, two of which are different from the prototypical 1 repeat:1 RNA base binding mode previously identified with model RNA sequences. RNA-binding affinities of PUM1 and PUM2 are not affected dramatically by the different binding modes in vitro. However, these modes of binding create structurally variable recognition surfaces that suggest a mechanism in vivo for recruitment of downstream effector proteins defined by the PUF:RNA complex.

Articles - 3q0r mentioned but not cited (1)



Reviews citing this publication (8)

  1. Functions, mechanisms and regulation of Pumilio/Puf family RNA binding proteins: a comprehensive review. Nishanth MJ, Simon B. Mol. Biol. Rep. 47 785-807 (2020)
  2. Post-transcriptional Regulatory Functions of Mammalian Pumilio Proteins. Goldstrohm AC, Hall TMT, McKenney KM. Trends Genet. 34 972-990 (2018)
  3. Engineering RNA-binding proteins with diverse activities. Wei H, Wang Z. Wiley Interdiscip Rev RNA 6 597-613 (2015)
  4. Engineering reprogrammable RNA-binding proteins for study and manipulation of the transcriptome. Abil Z, Zhao H. Mol Biosyst 11 2658-2665 (2015)
  5. Probing RNA-protein networks: biochemistry meets genomics. Campbell ZT, Wickens M. Trends Biochem. Sci. 40 157-164 (2015)
  6. Engineered proteins with Pumilio/fem-3 mRNA binding factor scaffold to manipulate RNA metabolism. Wang Y, Wang Z, Tanaka Hall TM. FEBS J. 280 3755-3767 (2013)
  7. Engineering RNA-binding proteins for biology. Chen Y, Varani G. FEBS J. 280 3734-3754 (2013)
  8. Repressive translational control in germ cells. Lai F, King ML. Mol. Reprod. Dev. 80 665-676 (2013)

Articles citing this publication (29)

  1. Specific and modular binding code for cytosine recognition in Pumilio/FBF (PUF) RNA-binding domains. Dong S, Wang Y, Cassidy-Amstutz C, Lu G, Bigler R, Jezyk MR, Li C, Hall TM, Wang Z. J. Biol. Chem. 286 26732-26742 (2011)
  2. A protein-RNA specificity code enables targeted activation of an endogenous human transcript. Campbell ZT, Valley CT, Wickens M. Nat. Struct. Mol. Biol. 21 732-738 (2014)
  3. The potential for manipulating RNA with pentatricopeptide repeat proteins. Yagi Y, Nakamura T, Small I. Plant J. 78 772-782 (2014)
  4. Drosophila Nanos acts as a molecular clamp that modulates the RNA-binding and repression activities of Pumilio. Weidmann CA, Qiu C, Arvola RM, Lou TF, Killingsworth J, Campbell ZT, Tanaka Hall TM, Goldstrohm AC. Elife 5 (2016)
  5. Modular assembly of designer PUF proteins for specific post-transcriptional regulation of endogenous RNA. Abil Z, Denard CA, Zhao H. J Biol Eng 8 7 (2014)
  6. Identification of a conserved interface between PUF and CPEB proteins. Campbell ZT, Menichelli E, Friend K, Wu J, Kimble J, Williamson JR, Wickens M. J. Biol. Chem. 287 18854-18862 (2012)
  7. Wild-Type U2AF1 Antagonizes the Splicing Program Characteristic of U2AF1-Mutant Tumors and Is Required for Cell Survival. Fei DL, Motowski H, Chatrikhi R, Prasad S, Yu J, Gao S, Kielkopf CL, Bradley RK, Varmus H. PLoS Genet. 12 e1006384 (2016)
  8. Nonspecific recognition is achieved in Pot1pC through the use of multiple binding modes. Dickey TH, McKercher MA, Wuttke DS. Structure 21 121-132 (2013)
  9. Depletion of the Trypanosome Pumilio domain protein PUF2 or of some other essential proteins causes transcriptome changes related to coding region length. Jha BA, Fadda A, Merce C, Mugo E, Droll D, Clayton C. Eukaryotic Cell 13 664-674 (2014)
  10. Programmable RNA-binding protein composed of repeats of a single modular unit. Adamala KP, Martin-Alarcon DA, Boyden ES. Proc. Natl. Acad. Sci. U.S.A. 113 E2579-88 (2016)
  11. A Quantitative and Predictive Model for RNA Binding by Human Pumilio Proteins. Jarmoskaite I, Denny SK, Vaidyanathan PP, Becker WR, Andreasson JOL, Layton CJ, Kappel K, Shivashankar V, Sreenivasan R, Das R, Greenleaf WJ, Herschlag D. Mol Cell 74 966-981.e18 (2019)
  12. RNA-binding specificity landscape of the pentatricopeptide repeat protein PPR10. Miranda RG, Rojas M, Montgomery MP, Gribbin KP, Barkan A. RNA 23 586-599 (2017)
  13. The trypanosome Pumilio domain protein PUF5. Jha BA, Archer SK, Clayton CE. PLoS ONE 8 e77371 (2013)
  14. Identification of diverse target RNAs that are functionally regulated by human Pumilio proteins. Bohn JA, Van Etten JL, Schagat TL, Bowman BM, McEachin RC, Freddolino PL, Goldstrohm AC. Nucleic Acids Res. 46 362-386 (2018)
  15. Programmable design of functional ribonucleoprotein complexes. Rath AK, Kellermann SJ, Rentmeister A. Chem Asian J 9 2045-2051 (2014)
  16. Pseudouridine and N6-methyladenosine modifications weaken PUF protein/RNA interactions. Vaidyanathan PP, AlSadhan I, Merriman DK, Al-Hashimi HM, Herschlag D. RNA 23 611-618 (2017)
  17. Structure-guided U2AF65 variant improves recognition and splicing of a defective pre-mRNA. Agrawal AA, McLaughlin KJ, Jenkins JL, Kielkopf CL. Proc. Natl. Acad. Sci. U.S.A. 111 17420-17425 (2014)
  18. Engineering specificity changes on a RanBP2 zinc finger that binds single-stranded RNA. Vandevenne M, O'Connell MR, Helder S, Shepherd NE, Matthews JM, Kwan AH, Segal DJ, Mackay JP. Angew. Chem. Int. Ed. Engl. 53 7848-7852 (2014)
  19. Expanding RNA binding specificity and affinity of engineered PUF domains. Zhao YY, Mao MW, Zhang WJ, Wang J, Li HT, Yang Y, Wang Z, Wu JW. Nucleic Acids Res. 46 4771-4782 (2018)
  20. SSMART: sequence-structure motif identification for RNA-binding proteins. Munteanu A, Mukherjee N, Ohler U. Bioinformatics 34 3990-3998 (2018)
  21. Engineering a conserved RNA regulatory protein repurposes its biological function in vivo. Bhat VD, McCann KL, Wang Y, Fonseca DR, Shukla T, Alexander JC, Qiu C, Wickens M, Lo TW, Tanaka Hall TM, Campbell ZT. Elife 8 (2019)
  22. PUM1 and PUM2 exhibit different modes of regulation for SIAH1 that involve cooperativity with NANOS paralogues. Sajek M, Janecki DM, Smialek MJ, Ginter-Matuszewska B, Spik A, Oczkowski S, Ilaslan E, Kusz-Zamelczyk K, Kotecki M, Blazewicz J, Jaruzelska J. Cell. Mol. Life Sci. 76 147-161 (2019)
  23. Structural basis for the specific recognition of 18S rRNA by APUM23. Bao H, Wang N, Wang C, Jiang Y, Liu J, Xu L, Wu J, Shi Y. Nucleic Acids Res. 45 12005-12014 (2017)
  24. Blind tests of RNA-protein binding affinity prediction. Kappel K, Jarmoskaite I, Vaidyanathan PP, Greenleaf WJ, Herschlag D, Das R. Proc. Natl. Acad. Sci. U.S.A. 116 8336-8341 (2019)
  25. Effects of PUMILIO1 and PUMILIO2 knockdown on cardiomyogenic differentiation of human embryonic stem cells culture. Silva ILZ, Robert AW, Cabo GC, Spangenberg L, Stimamiglio MA, Dallagiovanna B, Gradia DF, Shigunov P. PLoS One 15 e0222373 (2020)
  26. Nop9 recognizes structured and single-stranded RNA elements of preribosomal RNA. Zhang J, Teramoto T, Qiu C, Wine RN, Gonzalez LE, Baserga SJ, Tanaka Hall TM. RNA 26 1049-1059 (2020)
  27. Preparation of cooperative RNA recognition complexes for crystallographic structural studies. Qiu C, Goldstrohm AC, Tanaka Hall TM. Meth. Enzymol. 623 1-22 (2019)
  28. Principles of mRNA control by human PUM proteins elucidated from multimodal experiments and integrative data analysis. Wolfe MB, Schagat TL, Paulsen MT, Magnuson B, Ljungman M, Park D, Zhang C, Campbell ZT, Goldstrohm AC, Freddolino PL. RNA 26 1680-1703 (2020)
  29. Pumilio RNA recognition: the consequence of promiscuity. Ryder SP. Structure 19 277-279 (2011)