A dynamic intron retention program enriched in RNA processing genes regulates gene expression during terminal erythropoiesis

Nucleic Acids Research

Volumn 44, Issue 2, 2016, Pages 838-851

  Pimentel, Harold ^a   Parra, Marilyn ^b   Gee, Sherry L ^b   Mohandas, Narla ^c   Pachter, Lior ^a   Conboy, John G ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^c NEW YORK BLOOD CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FUSED IN SARCOMA PROTEIN; MESSENGER RNA; ACTIN BINDING PROTEIN; CATION TRANSPORT PROTEIN; JRAB PROTEIN, HUMAN; MFRN1 PROTEIN, HUMAN; MITOCHONDRIAL PROTEIN; PHOSPHOPROTEIN; RNA SPLICING; RNA SPLICING FACTOR; SF3B1 PROTEIN, HUMAN; SLC25A28 PROTEIN, HUMAN; SMALL NUCLEAR RIBONUCLEOPROTEIN; SPECTRIN; STOP CODON;

ARTICLE; CELL NUCLEUS; CELLULAR DISTRIBUTION; CLUSTER ANALYSIS; CONTROLLED STUDY; ERYTHROBLAST; ERYTHROPOIESIS; EXON; GENE; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; INTRON RETENTION; IRON BALANCE; NONSENSE MUTATION; PREMATURE TERMINATION CODON; PRIORITY JOURNAL; RNA PROCESSING; RNA SEQUENCE; RNA SPLICING; SF3B1 GENE; SLC25A28 GENE; SLC25A37 GENE; CELL CULTURE; CELL DIFFERENTIATION; CYTOLOGY; GENETICS; INTRON; NONSENSE MEDIATED MRNA DECAY; PHYSIOLOGY; STOP CODON;

CATION TRANSPORT PROTEINS; CELL DIFFERENTIATION; CELL NUCLEUS; CELLS, CULTURED; CLUSTER ANALYSIS; CODON, NONSENSE; ERYTHROBLASTS; ERYTHROPOIESIS; EXONS; GENE EXPRESSION REGULATION; HUMANS; INTRONS; MICROFILAMENT PROTEINS; MITOCHONDRIAL PROTEINS; NONSENSE MEDIATED MRNA DECAY; PHOSPHOPROTEINS; RIBONUCLEOPROTEIN, U2 SMALL NUCLEAR; RNA SPLICE SITES; RNA SPLICING FACTORS; SPECTRIN;

EID: 84966344016     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv1168     Document Type: Article

References (42)

1. An,X., Schulz,V.P., Li,J., Wu,K., Liu,J., Xue,F., Hu,J., Mohandas,N. and Gallagher,P.G. (2014) Global transcriptome analyses of human and murine terminal erythroid differentiation. Blood, 123, 3466-3477.
2. Pimentel,H., Parra,M., Gee,S., Ghanem,D., An,X., Li,J., Mohandas,N., Pachter,L. and Conboy,J.G. (2014) A dynamic alternative splicing program regulates gene expression during terminal erythropoiesis. Nucleic Acids Res., 42, 4031-4042.
3. Paralkar,V.R., Mishra,T., Luan,J., Yao,Y., Kossenkov,A.V., Anderson,S.M., Dunagin,M., Pimkin,M., Gore,M., Sun,D. et al. (2014) Lineage and species-specific long noncoding RNAs during erythro-megakaryocytic development. Blood, 123, 1927-1937.
4. Cheng,A.W., Shi,J., Wong,P., Luo,K.L., Trepman,P., Wang,E.T., Choi,H., Burge,C.B. and Lodish,H.F. (2014) Muscleblind-like 1 (Mbnl1) regulates pre-mRNA alternative splicing during terminal erythropoiesis. Blood, 124, 598-610.
5. Shi,L., Lin,Y.H., Sierant,M.C., Zhu,F., Cui,S., Guan,Y., Sartor,M.A., Tanabe,O., Lim,K.C. and Engel,J.D. (2014) Developmental transcriptome analysis of human erythropoiesis. Hum. Mol. Genet., 23, 4528-4542.
6. Chasis,J.A., Coulombel,L., Conboy,J., McGee,S., Andrews,K., Kan,Y.W. and Mohandas,N. (1993) Differentiation-associated switches in protein 4.1 expression. Synthesis of multiple structural isoforms during normal human erythropoiesis. J. Clin. Invest., 91, 329-338.
7. Discher,D., Parra,M., Conboy,J.G. and Mohandas,N. (1993) Mechanochemistry of the alternatively spliced spectrin-actin binding domain in membrane skeletal protein 4.1. J. Biol. Chem., 268, 7186-7195.
8. Horne,W.C., Huang,S.C., Becker,P.S., Tang,T.K. and Benz,E.J. Jr. (1993) Tissue-specific alternative splicing of protein 4.1 inserts an exon necessary for formation of the ternary complex with erythrocyte spectrin and F-actin. Blood, 82, 2558-2563.
9. Boutz,P.L., Bhutkar,A. and Sharp,P.A. (2015) Detained introns are a novel, widespread class of post-transcriptionally spliced introns. Genes Dev., 29, 63-80.
10. Cho,V., Mei,Y., Sanny,A., Chan,S., Enders,A., Bertram,E.M., Tan,A., Goodnow,C.C. and Andrews,T.D. (2014) The RNA-binding protein hnRNPLL induces a T cell alternative splicing program delineated by differential intron retention in polyadenylated RNA. Genome Biol., 15, R26.
11. Shalgi,R., Hurt,J.A., Krykbaeva,I., Taipale,M., Lindquist,S. and Burge,C.B. (2013) Widespread regulation of translation by elongation pausing in heat shock. Mol. Cell, 49, 439-452.
12. Wong,J.J., Ritchie,W., Ebner,O.A., Selbach,M., Wong,J.W., Huang,Y., Gao,D., Pinello,N., Gonzalez,M., Baidya,K. et al. (2013) Orchestrated intron retention regulates normal granulocyte differentiation. Cell, 154, 583-595.
13. Yap,K., Lim,Z.Q., Khandelia,P., Friedman,B. and Makeyev,E.V. (2012) Coordinated regulation of neuronal mRNA steady-state levels through developmentally controlled intron retention. Genes Dev., 26, 1209-1223.
14. Dvinge,H. and Bradley,R.K. (2015) Widespread intron retention diversifies most cancer transcriptomes. Genome Med., 7, 45.
15. Braunschweig,U., Barbosa-Morais,N.L., Pan,Q., Nachman,E.N., Alipanahi,B., Gonatopoulos-Pournatzis,T., Frey,B., Irimia,M. and Blencowe,B.J. (2014) Widespread intron retention in mammals functionally tunes transcriptomes. Genome Res., 24, 1774-1786.
16. Filichkin,S.A., Priest,H.D., Givan,S.A., Shen,R., Bryant,D.W., Fox,S.E., Wong,W.K. and Mockler,T.C. (2010) Genome-wide mapping of alternative splicing in Arabidopsis thaliana. Genome Res., 20, 45-58.
17. Ninomiya,K., Kataoka,N. and Hagiwara,M. (2011) Stress-responsive maturation of Clk1/4 pre-mRNAs promotes phosphorylation of SR splicing factor. J. Cell Biol., 195, 27-40.
18. Boothby,T.C., Zipper,R.S., van der Weele,C.M. and Wolniak,S.M. (2013) Removal of retained introns regulates translation in the rapidly developing gametophyte of Marsilea vestita. Dev. Cell, 24, 517-529.
19. Roberts,A. and Pachter,L. (2013) Streaming fragment assignment for real-time analysis of sequencing experiments. Nat. Methods, 10, 71-73.
20. Li,B., Ruotti,V., Stewart,R.M., Thomson,J.A. and Dewey,C.N. (2010) RNA-Seq gene expression estimation with read mapping uncertainty. Bioinformatics, 26, 493-500.
21. Huang,D.W., Sherman,B.T. and Lempicki,R.A. (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc., 4, 44-57.
22. Huang,D.W., Sherman,B.T. and Lempicki,R.A. (2009) Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res., 37, 1-13.
23. Yeo,G. and Burge,C.B. (2004) Maximum entropy modeling of short sequence motifs with applications to RNA splicing signals. J. Comput. Biol., 11, 377-394.
24. Hu,J., Liu,J., Xue,F., Halverson,G., Reid,M., Guo,A., Chen,L., Raza,A., Galili,N., Jaffray,J. et al. (2013) Isolation and functional characterization of human erythroblasts at distinct stages: implications for understanding of normal and disordered erythropoiesis in vivo. Blood, 121, 3246-3253.
25. Pandya-Jones,A. and Black,D.L. (2009) Co-transcriptional splicing of constitutive and alternative exons. RNA, 15, 1896-1908.
26. Schlaitz,A.L., Thompson,J., Wong,C.C., Yates,J.R. 3rd and Heald,R. (2013) REEP3/4 ensure endoplasmic reticulum clearance from metaphase chromatin and proper nuclear envelope architecture. Dev. Cell, 26, 315-323.
27. Reinecke,J.B., Katafiasz,D., Naslavsky,N. and Caplan,S. (2015) Novel functions for the endocytic regulatory proteins MICAL-L1 and EHD1 in mitosis. Traffic, 16, 48-67.
28. Lee,K. and Rhee,K. (2012) Separase-dependent cleavage of pericentrin B is necessary and sufficient for centriole disengagement during mitosis. Cell Cycle, 11, 2476-2485.
29. Pandya-Jones,A., Bhatt,D.M., Lin,C.H., Tong,A.J., Smale,S.T. and Black,D.L. (2013) Splicing kinetics and transcript release from the chromatin compartment limit the rate of Lipid A-induced gene expression. RNA, 19, 811-827.
30. Khodor,Y.L., Menet,J.S., Tolan,M. and Rosbash,M. (2012) Cotranscriptional splicing efficiency differs dramatically between Drosophila and mouse. RNA, 18, 2174-2186.
31. Lareau,L.F. and Brenner,S.E. (2015) Regulation of splicing factors by alternative splicing and NMD is conserved between kingdoms yet evolutionarily flexible. Mol. Biol. Evol., 32, 1072-1079.
32. Lareau,L.F., Inada,M., Green,R.E., Wengrod,J.C. and Brenner,S.E. (2007) Unproductive splicing of SR genes associated with highly conserved and ultraconserved DNA elements. Nature, 446, 926-929.
33. Chiou,N.T., Shankarling,G. and Lynch,K.W. (2013) hnRNP L and hnRNP A1 induce extended U1 snRNA interactions with an exon to repress spliceosome assembly. Mol. Cell, 49, 972-982.
34. Sharma,S., Maris,C., Allain,F.H. and Black,D.L. (2011) U1 snRNA directly interacts with polypyrimidine tract-binding protein during splicing repression. Mol. Cell, 41, 579-588.
35. Bonnal,S., Martinez,C., Forch,P., Bachi,A., Wilm,M. and Valcarcel,J. (2008) RBM5/Luca-15/H37 regulates Fas alternative splice site pairing after exon definition. Mol. Cell, 32, 81-95.
36. Cote,J., Dupuis,S., Jiang,Z. and Wu,J.Y. (2001) Caspase-2 pre-mRNA alternative splicing: identification of an intronic element containing a decoy 3′ acceptor site. Proc. Natl. Acad. Sci. U.S.A., 98, 938-943.
37. Eom,T., Zhang,C., Wang,H., Lay,K., Fak,J., Noebels,J.L. and Darnell,R.B. (2013) NOVA-dependent regulation of cryptic NMD exons controls synaptic protein levels after seizure. eLife, 2, e00178.
38. Zheng,S., Gray,E.E., Chawla,G., Porse,B.T., O'Dell,T.J. and Black,D.L. (2012) PSD-95 is post-transcriptionally repressed during early neural development by PTBP1 and PTBP2. Nat. Neurosci., 15, 381-388.
39. Acedo,A., Sanz,D.J., Duran,M., Infante,M., Perez-Cabornero,L., Miner,C. and Velasco,E.A. (2012) Comprehensive splicing functional analysis of DNA variants of the BRCA2 gene by hybrid minigenes. Breast Cancer Res., 14, R87.
40. Eswaran,J., Horvath,A., Godbole,S., Reddy,S.D., Mudvari,P., Ohshiro,K., Cyanam,D., Nair,S., Fuqua,S.A., Polyak,K. et al. (2013) RNA sequencing of cancer reveals novel splicing alterations. Sci. Rep., 3, 1689.
41. Madan,V., Kanojia,D., Li,J., Okamoto,R., Sato-Otsubo,A., Kohlmann,A., Sanada,M., Grossmann,V., Sundaresan,J., Shiraishi,Y. et al. (2015) Aberrant splicing of U12-type introns is the hallmark of ZRSR2 mutant myelodysplastic syndrome. Nat. Commun., 6, 6042.
42. Visconte,V., Avishai,N., Mahfouz,R., Tabarroki,A., Cowen,J., Sharghi-Moshtaghin,R., Hitomi,M., Rogers,H.J., Hasrouni,E., Phillips,J. et al. (2015) Distinct iron architecture in SF3B1-mutant myelodysplastic syndrome patients is linked to an SLC25A37 splice variant with a retained intron. Leukemia, 29, 188-195.