Repression of Pumilio Protein Expression by Rbfox1 Promotes Germ Cell Differentiation

Developmental Cell

Volumn 36, Issue 5, 2016, Pages 562-571

  Carreira Rosario, Arnaldo ^a   Bhargava, Varsha ^a   Hillebrand, Jens ^b   Kollipara, Rahul K ^a   Ramaswami, Mani ^b   Buszczak, Michael ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; RNA BINDING FOX PROTEIN; RNA BINDING PROTEIN; UNCLASSIFIED DRUG; DROSOPHILA PROTEIN; RBFOX1 PROTEIN, DROSOPHILA;

3' UNTRANSLATED REGION; ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL MATURATION; CONTROLLED STUDY; CYST; CYTOPLASM; DROSOPHILA; FEMALE; GENE SILENCING; GERM CELL; NEOPLASM; NONHUMAN; OVARY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA TRANSLATION; ALTERNATIVE RNA SPLICING; ANIMAL; CYTOLOGY; DROSOPHILA MELANOGASTER; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY;

ALTERNATIVE SPLICING; ANIMALS; CELL DIFFERENTIATION; CYTOPLASM; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GERM CELLS; OVARY; RNA, MESSENGER; RNA-BINDING PROTEINS;

EID: 84959270062     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2016.02.010     Document Type: Article

References (44)

1. Auweter S.D., Fasan R., Reymond L., Underwood J.G., Black D.L., Pitsch S., Allain F.H. Molecular basis of RNA recognition by the human alternative splicing factor Fox-1. EMBO J. 2006, 25:163-173.
2. Barnby G., Abbott A., Sykes N., Morris A., Weeks D.E., Mott R., Lamb J., Bailey A.J., Monaco A.P. Candidate-gene screening and association analysis at the autism-susceptibility locus on chromosome 16p: evidence of association at GRIN2A and ABAT. Am. J. Hum. Genet. 2005, 76:950-966. International Molecular Genetics Study of Autism Consortium.
3. Bhalla K., Phillips H.A., Crawford J., McKenzie O.L.D., Mulley J.C., Eyre H., Gardner A.E., Kremmidiotis G., Callen D.F. The de novo chromosome 16 translocations of two patients with abnormal phenotypes (mental retardation and epilepsy) disrupt the A2BP1 gene. J. Hum. Genet. 2004, 49:308-311.
4. Braunschweig U., Gueroussov S., Plocik A.M., Graveley B.R., Blencowe B.J. Dynamic integration of splicing within gene regulatory pathways. Cell 2013, 152:1252-1269.
5. Brawley C., Matunis E. Regeneration of male germline stem cells by spermatogonial dedifferentiation in vivo. Science 2004, 304:1331-1334.
6. Buszczak M., Spradling A.C. The Drosophila P68 RNA helicase regulates transcriptional deactivation by promoting RNA release from chromatin. Genes Dev. 2006, 20:977-989.
7. Carreira-Rosario A., Scoggin S., Shalaby N.A., Williams N.D., Hiesinger P.R., Buszczak M. Recombineering homologous recombination constructs in Drosophila. J. Vis. Exp. 2013, e50346.
8. Chau J., Kulnane L.S., Salz H.K. Sex-lethal facilitates the transition from germline stem cell to committed daughter cell in the Drosophila ovary. Genetics 2009, 182:121-132.
9. Chau J., Kulnane L.S., Salz H.K. Sex-lethal enables germline stem cell differentiation by down-regulating Nanos protein levels during Drosophila oogenesis. Proc. Natl. Acad. Sci. USA 2012, 109:9465-9470.
10. Das S., Sadanandappa M.K., Dervan A., Larkin A., Lee J.A., Sudhakaran I.P., Priya R., Heidari R., Holohan E.E., Pimentel A., et al. Plasticity of local GABAergic interneurons drives olfactory habituation. Proc. Natl. Acad. Sci. USA 2011, 108:E646-E654.
11. Davis L.K., Maltman N., Mosconi M.W., Macmillan C., Schmitt L., Moore K., Francis S.M., Jacob S., Sweeney J.A., Cook E.H. Rare inherited A2BP1 deletion in a proband with autism and developmental hemiparesis. Am. J. Med. Genet. A 2012, 158A:1654-1661.
12. de Cuevas M., Spradling A.C. Morphogenesis of the Drosophila fusome and its implications for oocyte specification. Development 1998, 125:2781-2789.
13. Dredge B.K., Jensen K.B. NeuN/Rbfox3 nuclear and cytoplasmic isoforms differentially regulate alternative splicing and nonsense-mediated decay of Rbfox2. PLoS One 2011, 6:e21585.
14. 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.
15. Gehman L.T., Stoilov P., Maguire J., Damianov A., Lin C.-H., Shiue L., Ares M., Mody I., Black D.L. The splicing regulator Rbfox1 (A2BP1) controls neuronal excitation in the mammalian brain. Nat. Genet. 2011, 43:706-711.
16. Gehman L.T., Meera P., Stoilov P., Shiue L., O'Brien J.E., Meisler M.H., Ares M., Otis T.S., Black D.L. The splicing regulator Rbfox2 is required for both cerebellar development and mature motor function. Genes Dev. 2012, 26:445-460.
17. Gratz S.J., Cummings A.M., Nguyen J.N., Hamm D.C., Donohue L.K., Harrison M.M., Wildonger J., O'Connor-Giles K.M. Genome engineering of Drosophila with the CRISPR RNA-guided Cas9 nuclease. Genetics 2013, 194:1029-1035.
18. Gratz S.J., Ukken F.P., Rubinstein C.D., Thiede G., Donohue L.K., Cummings A.M., O'Connor-Giles K.M. Highly specific and efficient CRISPR/Cas9-catalyzed homology-directed repair in Drosophila. Genetics 2014, 196:961-971.
19. Hamada N., Ito H., Iwamoto I., Mizuno M., Morishita R., Inaguma Y., Kawamoto S., Tabata H., Nagata K. Biochemical and morphological characterization of A2BP1 in neuronal tissue. J. Neurosci. Res. 2013, 91:1303-1311.
20. Hu J., Ho A.L., Yuan L., Hu B., Hua S., Hwang S.S., Zhang J., Hu T., Zheng H., Gan B., et al. From the Cover: neutralization of terminal differentiation in gliomagenesis. Proc. Natl. Acad. Sci. USA 2013, 110:14520-14527.
21. Jin Y., Suzuki H., Maegawa S., Endo H., Sugano S., Hashimoto K., Yasuda K., Inoue K. A vertebrate RNA-binding protein Fox-1 regulates tissue-specific splicing via the pentanucleotide GCAUG. EMBO J. 2003, 22:905-912.
22. Joly W., Chartier A., Rojas-Rios P., Busseau I., Simonelig M. 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 Rep. 2013, 1:411-424.
23. Kai T., Spradling A. Differentiating germ cells can revert into functional stem cells in Drosophila melanogaster ovaries. Nature 2004, 428:564-569.
24. Kiehl T.R., Shibata H., Vo T., Huynh D.P., Pulst S.M. Identification and expression of a mouse ortholog of A2BP1. Mamm. Genome 2001, 12:595-601.
25. Kim K.K., Adelstein R.S., Kawamoto S. Identification of neuronal nuclei (NeuN) as Fox-3, a new member of the Fox-1 gene family of splicing factors. J. Biol. Chem. 2009, 284:31052-31061.
26. Kim G., Pai C.I., Sato K., Person M.D., Nakamura A., Macdonald P.M. Region-specific activation of oskar mRNA translation by inhibition of Bruno-mediated repression. PLoS Genet. 2015, 11:e1004992.
27. Kuroyanagi H. Fox-1 family of RNA-binding proteins. Cell Mol. Life Sci. 2009, 66:3895-3907.
28. Lee J.A., Tang Z.Z., Black D.L. An inducible change in Fox-1/A2BP1 splicing modulates the alternative splicing of downstream neuronal target exons. Genes Dev. 2009, 23:2284-2293.
29. Lee J.A., Damianov A., Lin C.H., Fontes M., Parikshak N.N., Anderson E.S., Geschwind D.H., Black D.L., Martin K.C. Cytoplasmic Rbfox1 regulates the expression of synaptic and autism-related genes. Neuron 2016, 89:113-128.
30. Li Y., Maines J.Z., Tastan O.Y., McKearin D.M., Buszczak M. Mei-P26 regulates the maintenance of ovarian germline stem cells by promoting BMP signaling. Development 2012, 139:1547-1556.
31. Lukong K.E., Chang K.W., Khandjian E.W., Richard S. RNA-binding proteins in human genetic disease. Trends Genet. 2008, 24:416-425.
32. Menon K.P., Sanyal S., Habara Y., Sanchez R., Wharton R.P., 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.
33. Mikhail F.M., Lose E.J., Robin N.H., Descartes M.D., Rutledge K.D., Rutledge S.L., Korf B.R., Carroll A.J. Clinically relevant single gene or intragenic deletions encompassing critical neurodevelopmental genes in patients with developmental delay, mental retardation, and/or autism spectrum disorders. Am. J. Med. Genet. A 2011, 155A:2386-2396.
34. Ni J.Q., Zhou R., Czech B., Liu L.P., Holderbaum L., Yang-Zhou D., Shim H.S., Tao R., Handler D., Karpowicz P., et al. A genome-scale shRNA resource for transgenic RNAi in Drosophila. Nat. Methods 2011, 8:405-407.
35. Pfeiffer B.D., Truman J.W., Rubin G.M. Using translational enhancers to increase transgene expression in Drosophila. Proc. Natl. Acad. Sci. USA 2012, 109:6626-6631.
36. Ponthier J.L., Schluepen C., Chen W., Lersch R.A., Gee S.L., Hou V.C., Lo A.J., Short S.A., Chasis J.A., Winkelmann J.C., Conboy J.G. Fox-2 splicing factor binds to a conserved intron motif to promote inclusion of protein 4.1R alternative exon 16. J. Biol. Chem. 2006, 281:12468-12474.
37. Ramaswami M., Taylor J.P., Parker R. Altered ribostasis: RNA-protein granules in degenerative disorders. Cell 2013, 154:727-736.
38. Sebat J., Lakshmi B., Malhotra D., Troge J., Lese-Martin C., Walsh T., Yamrom B., Yoon S., Krasnitz A., Kendall J., et al. Strong association of de novo copy number mutations with autism. Science 2007, 316:445-449.
39. Sengupta N., Yau C., Sakthianandeswaren A., Mouradov D., Gibbs P., Suraweera N., Cazier J.B., Polanco-Echeverry G., Ghosh A., Thaha M., et al. Analysis of colorectal cancers in British Bangladeshi identifies early onset, frequent mucinous histotype and a high prevalence of RBFOX1 deletion. Mol. Cancer 2013, 12:1.
40. Sheng X.R., Brawley C.M., Matunis E.L. Dedifferentiating spermatogonia outcompete somatic stem cells for niche occupancy in the Drosophila testis. Cell Stem Cell 2009, 5:191-203.
41. Shibata H., Huynh D.P., Pulst S.-M. A novel protein with RNA-binding motifs interacts with ataxin-2. Hum. Mol. Genet. 2000, 9:1303-1313.
42. Slaidina M., Lehmann R. Translational control in germline stem cell development. J. Cell Biol. 2014, 207:13-21.
43. Tastan Ö.Y., Maines J.Z., Li Y., Mckearin D.M., Buszczak M. Drosophila Ataxin 2-binding protein 1 marks an intermediate step in the molecular differentiation of female germline cysts. Development 2010, 137:3167-3176.
44. Weyn-Vanhentenryck S.M., Mele A., Yan Q., Sun S., Farny N., Zhang Z., Xue C., Herre M., Silver P.A., Zhang M.Q., et al. HITS-CLIP and integrative modeling define the Rbfox splicing-regulatory network linked to brain development and autism. Cell Rep. 2014, 6:1139-1152.