Building robust transcriptomes with master splicing factors

Cell

Volumn 159, Issue 3, 2014, Pages 487-498

  Jangi, Mohini ^a   Sharp, Phillip A ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN L; MESSENGER RNA PRECURSOR; MUSCLEBLIND LIKE 1 PROTEIN; NOVA1 PROTEIN; NOVA2 PROTEIN; OCTAMER TRANSCRIPTION FACTOR 4; POLYPYRIMIDINE TRACT BINDING PROTEIN; POLYPYRIMIDINE TRACT BINDING PROTEIN 2; PROTEIN; RBFOX2 PROTEIN; RBM38 PROTEIN; RNA BINDING PROTEIN; SERINE ARGININE RICH PROTEIN; TRANSCRIPTOME; UNCLASSIFIED DRUG; TRANSCRIPTION FACTOR;

ALTERNATIVE RNA SPLICING; AUTOREGULATION; BINDING SITE; CELL STRESS; CELL SURVIVAL; DNA BINDING; EMBRYONIC STEM CELL; ENHANCER REGION; EPITHELIAL MESENCHYMAL TRANSITION; FIBROBLAST; GENE OVEREXPRESSION; GENE PRODUCT; GENETIC CONSERVATION; HEMATOPOIETIC CELL; HOMEOSTASIS; HUMAN; HYPEROSMOTIC STRESS; INTRON; LONG TERM POTENTIATION; MUSCLE DEVELOPMENT; MYOBLAST; NERVE CELL DIFFERENTIATION; NERVE CELL PLASTICITY; NONHUMAN; NONSENSE MEDIATED MRNA DECAY; NUCLEAR REPROGRAMMING; POSITIVE FEEDBACK; PROTEIN RNA BINDING; REVIEW; SEX DETERMINATION; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; STEADY STATE; T LYMPHOCYTE ACTIVATION; TRANSCRIPTION INITIATION; UPREGULATION; ANIMAL; ANTIBODY SPECIFICITY; FEEDBACK SYSTEM; GENE EXPRESSION REGULATION; METABOLISM; RNA SPLICING;

ALTERNATIVE SPLICING; ANIMALS; FEEDBACK; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMEOSTASIS; HUMANS; ORGAN SPECIFICITY; RNA SPLICING; RNA-BINDING PROTEINS; TRANSCRIPTION FACTORS; TRANSCRIPTOME;

EID: 84908284686     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2014.09.054     Document Type: Review

References (100)

1. U. Alon An Introduction to Systems Biology: Design Principles of Biological Circuits 2006 CRC Press Boca Raton, Florida
2. U. Alon Network motifs: theory and experimental approaches Nat. Rev. Genet. 8 2007 450 461
3. M.L. Änkö, M. Müller-McNicoll, H. Brandl, T. Curk, C. Gorup, I. Henry, J. Ule, and K.M. Neugebauer The RNA-binding landscapes of two SR proteins reveal unique functions and binding to diverse RNA classes Genome Biol. 13 2012 R17
4. D. Baek, and P. Green Sequence conservation, relative isoform frequencies, and nonsense-mediated decay in evolutionarily conserved alternative splicing Proc. Natl. Acad. Sci. USA 102 2005 12813 12818
5. Y. Barash, J.A. Calarco, W. Gao, Q. Pan, X. Wang, O. Shai, B.J. Blencowe, and B.J. Frey Deciphering the splicing code Nature 465 2010 53 59
6. N.L. Barbosa-Morais, M. Irimia, Q. Pan, H.Y. Xiong, S. Gueroussov, L.J. Lee, V. Slobodeniuc, C. Kutter, S. Watt, and R. Colak The evolutionary landscape of alternative splicing in vertebrate species Science 338 2012 1587 1593
7. G.J. Bashaw, and B.S. Baker The msl-2 dosage compensation gene of Drosophila encodes a putative DNA-binding protein whose expression is sex specifically regulated by Sex-lethal Development 121 1995 3245 3258
8. A. Becskei, and L. Serrano Engineering stability in gene networks by autoregulation Nature 405 2000 590 593
9. A. Becskei, B. Séraphin, and L. Serrano Positive feedback in eukaryotic gene networks: cell differentiation by graded to binary response conversion EMBO J. 20 2001 2528 2535
10. L.R. Bell, J.I. Horabin, P. Schedl, and T.W. Cline Positive autoregulation of sex-lethal by alternative splicing maintains the female determined state in Drosophila Cell 65 1991 229 239
11. D.M. Bhatt, A. Pandya-Jones, A.J. Tong, I. Barozzi, M.M. Lissner, G. Natoli, D.L. Black, and S.T. Smale Transcript dynamics of proinflammatory genes revealed by sequence analysis of subcellular RNA fractions Cell 150 2012 279 290
12. W.J. Blake, M. KAErn, C.R. Cantor, and J.J. Collins Noise in eukaryotic gene expression Nature 422 2003 633 637
13. P.L. Boutz, P. Stoilov, Q. Li, C.H. Lin, G. Chawla, K. Ostrow, L. Shiue, M. Ares Jr., and D.L. Black A post-transcriptional regulatory switch in polypyrimidine tract-binding proteins reprograms alternative splicing in developing neurons Genes Dev. 21 2007 1636 1652
14. J.A. Calarco, S. Superina, D. O'Hanlon, M. Gabut, B. Raj, Q. Pan, U. Skalska, L. Clarke, D. Gelinas, and D. van der Kooy Regulation of vertebrate nervous system alternative splicing and development by an SR-related protein Cell 138 2009 898 910
15. S.M. Carlson, C.R. Chouinard, A. Labadorf, C.J. Lam, K. Schmelzle, E. Fraenkel, and F.M. White Large-scale discovery of ERK2 substrates identifies ERK-mediated transcriptional regulation by ETV3 Sci. Signal. 4 2011 rs11
16. T.A. Cooper, L. Wan, and G. Dreyfuss RNA and disease Cell 136 2009 777 793
17. K.T. Coschigano, and P.C. Wensink Sex-specific transcriptional regulation by the male and female doublesex proteins of Drosophila Genes Dev. 7 1993 42 54
18. T.O. Crawford, and C.A. Pardo The neurobiology of childhood spinal muscular atrophy Neurobiol. Dis. 3 1996 97 110
19. A. Damianov, and D.L. Black Autoregulation of Fox protein expression to produce dominant negative splicing factors RNA 16 2010 405 416
20. P. de la Grange, L. Gratadou, M. Delord, M. Dutertre, and D. Auboeuf Splicing factor and exon profiling across human tissues Nucleic Acids Res. 38 2010 2825 2838
21. M.M. Denis, N.D. Tolley, M. Bunting, H. Schwertz, H. Jiang, S. Lindemann, C.C. Yost, F.J. Rubner, K.H. Albertine, and K.J. Swoboda Escaping the nuclear confines: signal-dependent pre-mRNA splicing in anucleate platelets Cell 122 2005 379 391
22. M. Gabut, P. Samavarchi-Tehrani, X. Wang, V. Slobodeniuc, D. O'Hanlon, H.K. Sung, M. Alvarez, S. Talukder, Q. Pan, and E.O. Mazzoni An alternative splicing switch regulates embryonic stem cell pluripotency and reprogramming Cell 147 2011 132 146
23. L.T. Gehman, P. Meera, P. Stoilov, L. Shiue, J.E. O'Brien, M.H. Meisler, M. Ares Jr., T.S. Otis, and D.L. Black The splicing regulator Rbfox2 is required for both cerebellar development and mature motor function Genes Dev. 26 2012 445 460
24. J. Giudice, Z. Xia, E.T. Wang, M.A. Scavuzzo, A.J. Ward, A. Kalsotra, W. Wang, X.H. Wehrens, C.B. Burge, and W. Li Alternative splicing regulates vesicular trafficking genes in cardiomyocytes during postnatal heart development Nat. Commun. 5 2014 3603
25. A.R. Grosso, A.Q. Gomes, N.L. Barbosa-Morais, S. Caldeira, N.P. Thorne, G. Grech, M. von Lindern, and M. Carmo-Fonseca Tissue-specific splicing factor gene expression signatures Nucleic Acids Res. 36 2008 4823 4832
26. H. Han, M. Irimia, P.J. Ross, H.K. Sung, B. Alipanahi, L. David, A. Golipour, M. Gabut, I.P. Michael, and E.N. Nachman MBNL proteins repress ES-cell-specific alternative splicing and reprogramming Nature 498 2013 241 245
27. S. Hao, and D. Baltimore RNA splicing regulates the temporal order of TNF-induced gene expression Proc. Natl. Acad. Sci. USA 110 2013 11934 11939
28. L.A. Heinicke, B. Nabet, S. Shen, P. Jiang, S. van Zalen, B. Cieply, J.E. Russell, Y. Xing, and R.P. Carstens The RNA binding protein RBM38 (RNPC1) regulates splicing during late erythroid differentiation PLoS ONE 8 2013 e78031
29. K.J. Hertel, K.W. Lynch, E.C. Hsiao, E.H. Liu, and T. Maniatis Structural and functional conservation of the Drosophila doublesex splicing enhancer repeat elements RNA 2 1996 969 981
30. F. Heyd, and K.W. Lynch Degrade, move, regroup: signaling control of splicing proteins Trends Biochem. Sci. 36 2011 397 404
31. D. Hnisz, B.J. Abraham, T.I. Lee, A. Lau, V. Saint-André, A.A. Sigova, H.A. Hoke, and R.A. Young Super-enhancers in the control of cell identity and disease Cell 155 2013 934 947
32. N. Holmes Immunology. A splicing switch for T cells Science 321 2008 646 647
33. C.S. Huang, S.H. Shi, J. Ule, M. Ruggiu, L.A. Barker, R.B. Darnell, Y.N. Jan, and L.Y. Jan Common molecular pathways mediate long-term potentiation of synaptic excitation and slow synaptic inhibition Cell 123 2005 105 118
34. S.C. Huelga, A.Q. Vu, J.D. Arnold, T.Y. Liang, P.P. Liu, B.Y. Yan, J.P. Donohue, L. Shiue, S. Hoon, and S. Brenner Integrative genome-wide analysis reveals cooperative regulation of alternative splicing by hnRNP proteins Cell Rep. 1 2012 167 178
35. J.Y. Ip, D. Schmidt, Q. Pan, A.K. Ramani, A.G. Fraser, D.T. Odom, and B.J. Blencowe Global impact of RNA polymerase II elongation inhibition on alternative splicing regulation Genome Res. 21 2011 390 401
36. M. Jangi, P.L. Boutz, P. Paul, and P.A. Sharp Rbfox2 controls autoregulation in RNA-binding protein networks Genes Dev. 28 2014 637 651
37. C.S. Jayasena, and M.E. Bronner Rbms3 functions in craniofacial development by posttranscriptionally modulating TGF-β signaling J. Cell Biol. 199 2012 453 466
38. K.B. Jensen, B.K. Dredge, G. Stefani, R. Zhong, R.J. Buckanovich, H.J. Okano, Y.Y. Yang, and R.B. Darnell Nova-1 regulates neuron-specific alternative splicing and is essential for neuronal viability Neuron 25 2000 359 371
39. Y. Jin, H. Suzuki, S. Maegawa, H. Endo, S. Sugano, K. Hashimoto, K. Yasuda, and K. Inoue A vertebrate RNA-binding protein Fox-1 regulates tissue-specific splicing via the pentanucleotide GCAUG EMBO J. 22 2003 905 912
40. D. Jin, K. Hidaka, M. Shirai, and T. Morisaki RNA-binding motif protein 24 regulates myogenin expression and promotes myogenic differentiation Genes Cells. 15 2010 1158 1167
41. A. Kalsotra, X. Xiao, A.J. Ward, J.C. Castle, J.M. Johnson, C.B. Burge, and T.A. Cooper A postnatal switch of CELF and MBNL proteins reprograms alternative splicing in the developing heart Proc. Natl. Acad. Sci. USA 105 2008 20333 20338
42. L.N. Keyes, T.W. Cline, and P. Schedl The primary sex determination signal of Drosophila acts at the level of transcription Cell 68 1992 933 943
43. H. Kitano Biological robustness Nat. Rev. Genet. 5 2004 826 837
44. N.M. Kuyumcu-Martinez, G.S. Wang, and T.A. Cooper Increased steady-state levels of CUGBP1 in myotonic dystrophy 1 are due to PKC-mediated hyperphosphorylation Mol. Cell 28 2007 68 78
45. L.F. Lareau, M. Inada, R.E. Green, J.C. Wengrod, and S.E. Brenner Unproductive splicing of SR genes associated with highly conserved and ultraconserved DNA elements Nature 446 2007 926 929
46. J.A. Lee, Z.Z. Tang, and D.L. Black An inducible change in Fox-1/A2BP1 splicing modulates the alternative splicing of downstream neuronal target exons Genes Dev. 23 2009 2284 2293
47. B.P. Lewis, R.E. Green, and S.E. Brenner Evidence for the widespread coupling of alternative splicing and nonsense-mediated mRNA decay in humans Proc. Natl. Acad. Sci. USA 100 2003 189 192
48. H.Y. Li, A. Bourdelas, C. Carron, and D.L. Shi The RNA-binding protein Seb4/RBM24 is a direct target of MyoD and is required for myogenesis during Xenopus early development Mech. Dev. 127 2010 281 291
49. D.D. Licatalosi, M. Yano, J.J. Fak, A. Mele, S.E. Grabinski, C. Zhang, and R.B. Darnell Ptbp2 represses adult-specific splicing to regulate the generation of neuronal precursors in the embryonic brain Genes Dev. 26 2012 1626 1642
50. J. Lim, T. Hao, C. Shaw, A.J. Patel, G. Szabó, J.F. Rual, C.J. Fisk, N. Li, A. Smolyar, and D.E. Hill A protein-protein interaction network for human inherited ataxias and disorders of Purkinje cell degeneration Cell 125 2006 801 814
51. K.H. Lim, L. Ferraris, M.E. Filloux, B.J. Raphael, and W.G. Fairbrother Using positional distribution to identify splicing elements and predict pre-mRNA processing defects in human genes Proc. Natl. Acad. Sci. USA 108 2011 11093 11098
52. W.A. Linke, and S. Bücker King of hearts: a splicing factor rules cardiac proteins Nat. Med. 18 2012 660 661
53. J.C. Long, and J.F. Caceres The SR protein family of splicing factors: master regulators of gene expression Biochem. J. 417 2009 15 27
54. Y. Lu, Y.H. Loh, H. Li, M. Cesana, S.B. Ficarro, J.R. Parikh, N. Salomonis, C.X. Toh, S.T. Andreadis, and C.J. Luckey Alternative splicing of MBD2 supports self-renewal in human pluripotent stem cells Cell Stem Cell 15 2014 92 101
55. K.W. Lynch, and T. Maniatis Assembly of specific SR protein complexes on distinct regulatory elements of the Drosophila doublesex splicing enhancer Genes Dev. 10 1996 2089 2101
56. Y.T. Maeda, and M. Sano Regulatory dynamics of synthetic gene networks with positive feedback J. Mol. Biol. 359 2006 1107 1124
57. E.V. Makeyev, J. Zhang, M.A. Carrasco, and T. Maniatis The MicroRNA miR-124 promotes neuronal differentiation by triggering brain-specific alternative pre-mRNA splicing Mol. Cell 27 2007 435 448
58. R. Martinez-Contreras, P. Cloutier, L. Shkreta, J.F. Fisette, T. Revil, and B. Chabot hnRNP proteins and splicing control Adv. Exp. Med. Biol. 623 2007 123 147
59. J.T. Mendell, N.A. Sharifi, J.L. Meyers, F. Martinez-Murillo, and H.C. Dietz Nonsense surveillance regulates expression of diverse classes of mammalian transcripts and mutes genomic noise Nat. Genet. 36 2004 1073 1078
60. J. Merkin, C. Russell, P. Chen, and C.B. Burge Evolutionary dynamics of gene and isoform regulation in Mammalian tissues Science 338 2012 1593 1599
61. J.E. Mermoud, P.T. Cohen, and A.I. Lamond Regulation of mammalian spliceosome assembly by a protein phosphorylation mechanism EMBO J. 13 1994 5679 5688
62. S. Miyamoto, K. Hidaka, D. Jin, and T. Morisaki RNA-binding proteins Rbm38 and Rbm24 regulate myogenic differentiation via p21-dependent and -independent regulatory pathways Genes Cells 14 2009 1241 1252
63. T. Nakaya, P. Alexiou, M. Maragkakis, A. Chang, and Z. Mourelatos FUS regulates genes coding for RNA-binding proteins in neurons by binding to their highly conserved introns RNA 19 2013 498 509
64. D. Nevozhay, R.M. Adams, K.F. Murphy, K. Josic, and G. Balázsi Negative autoregulation linearizes the dose-response and suppresses the heterogeneity of gene expression Proc. Natl. Acad. Sci. USA 106 2009 5123 5128
65. J.Z. Ni, L. Grate, J.P. Donohue, C. Preston, N. Nobida, G. O'Brien, L. Shiue, T.A. Clark, J.E. Blume, and M. Ares Jr. Ultraconserved elements are associated with homeostatic control of splicing regulators by alternative splicing and nonsense-mediated decay Genes Dev. 21 2007 708 718
66. K. Ninomiya, N. Kataoka, and M. Hagiwara Stress-responsive maturation of Clk1/4 pre-mRNAs promotes phosphorylation of SR splicing factor J. Cell Biol. 195 2011 27 40
67. S. Oberdoerffer, L.F. Moita, D. Neems, R.P. Freitas, N. Hacohen, and A. Rao Regulation of CD45 alternative splicing by heterogeneous ribonucleoprotein, hnRNPLL Science 321 2008 686 691
68. B. Raj, D. O'Hanlon, J.P. Vessey, Q. Pan, D. Ray, N.J. Buckley, F.D. Miller, and B.J. Blencowe Cross-regulation between an alternative splicing activator and a transcription repressor controls neurogenesis Mol. Cell 43 2011 843 850
69. R.F. Roscigno, and M.A. Garcia-Blanco SR proteins escort the U4/U6.U5 tri-snRNP to the spliceosome RNA 1 1995 692 706
70. N. Rosenfeld, M.B. Elowitz, and U. Alon Negative autoregulation speeds the response times of transcription networks J. Mol. Biol. 323 2002 785 793
71. O. Rossbach, L.H. Hung, S. Schreiner, I. Grishina, M. Heiner, J. Hui, and A. Bindereif Auto- and cross-regulation of the hnRNP L proteins by alternative splicing Mol. Cell. Biol. 29 2009 1442 1451
72. A.L. Saltzman, Y.K. Kim, Q. Pan, M.M. Fagnani, L.E. Maquat, and B.J. Blencowe Regulation of multiple core spliceosomal proteins by alternative splicing-coupled nonsense-mediated mRNA decay Mol. Cell. Biol. 28 2008 4320 4330
73. A.L. Saltzman, Q. Pan, and B.J. Blencowe Regulation of alternative splicing by the core spliceosomal machinery Genes Dev. 25 2011 373 384
74. H.K. Salz Sex determination in insects: a binary decision based on alternative splicing Curr. Opin. Genet. Dev. 21 2011 395 400
75. C. Schütt, and R. Nöthiger Structure, function and evolution of sex-determining systems in Dipteran insects Development 127 2000 667 677
76. I.M. Shapiro, A.W. Cheng, N.C. Flytzanis, M. Balsamo, J.S. Condeelis, M.H. Oktay, C.B. Burge, and F.B. Gertler An EMT-driven alternative splicing program occurs in human breast cancer and modulates cellular phenotype PLoS Genet. 7 2011 e1002218
77. S.G. Siera, and T.W. Cline Sexual back talk with evolutionary implications: stimulation of the Drosophila sex-determination gene sex-lethal by its target transformer Genetics 180 2008 1963 1981
78. B.A. Sosnowski, J.M. Belote, and M. McKeown Sex-specific alternative splicing of RNA from the transformer gene results from sequence-dependent splice site blockage Cell 58 1989 449 459
79. R. Spellman, M. Llorian, and C.W. Smith Crossregulation and functional redundancy between the splicing regulator PTB and its paralogs nPTB and ROD1 Mol. Cell 27 2007 420 434
80. M. Tian, and T. Maniatis A splicing enhancer complex controls alternative splicing of doublesex pre-mRNA Cell 74 1993 105 114
81. J.D. Topp, J. Jackson, A.A. Melton, and K.W. Lynch A cell-based screen for splicing regulators identifies hnRNP LL as a distinct signal-induced repressor of CD45 variable exon 4 RNA 14 2008 2038 2049
82. J. Ule, A. Ule, J. Spencer, A. Williams, J.S. Hu, M. Cline, H. Wang, T. Clark, C. Fraser, and M. Ruggiu Nova regulates brain-specific splicing to shape the synapse Nat. Genet. 37 2005 844 852
83. J. Ule, G. Stefani, A. Mele, M. Ruggiu, X. Wang, B. Taneri, T. Gaasterland, B.J. Blencowe, and R.B. Darnell An RNA map predicting Nova-dependent splicing regulation Nature 444 2006 580 586
84. J.P. Venables, R. Klinck, C. Koh, J. Gervais-Bird, A. Bramard, L. Inkel, M. Durand, S. Couture, U. Froehlich, and E. Lapointe Cancer-associated regulation of alternative splicing Nat. Struct. Mol. Biol. 16 2009 670 676
85. J.P. Venables, L. Lapasset, G. Gadea, P. Fort, R. Klinck, M. Irimia, E. Vignal, P. Thibault, P. Prinos, and B. Chabot MBNL1 and RBFOX2 cooperate to establish a splicing programme involved in pluripotent stem cell differentiation Nat. Commun. 4 2013 2480
86. C.H. Waddington The Strategy of the Genes 1957 George Allen and Unwin London
87. E.T. Wang, R. Sandberg, S. Luo, I. Khrebtukova, L. Zhang, C. Mayr, S.F. Kingsmore, G.P. Schroth, and C.B. Burge Alternative isoform regulation in human tissue transcriptomes Nature 456 2008 470 476
88. E.T. Wang, N.A. Cody, S. Jog, M. Biancolella, T.T. Wang, D.J. Treacy, S. Luo, G.P. Schroth, D.E. Housman, and S. Reddy Transcriptome-wide regulation of pre-mRNA splicing and mRNA localization by muscleblind proteins Cell 150 2012 710 724
89. J. Weischenfeldt, J. Waage, G. Tian, J. Zhao, I. Damgaard, J.S. Jakobsen, K. Kristiansen, A. Krogh, J. Wang, and B.T. Porse Mammalian tissues defective in nonsense-mediated mRNA decay display highly aberrant splicing patterns Genome Biol. 13 2012 R35
90. W.A. Whyte, D.A. Orlando, D. Hnisz, B.J. Abraham, C.Y. Lin, M.H. Kagey, P.B. Rahl, T.I. Lee, and R.A. Young Master transcription factors and mediator establish super-enhancers at key cell identity genes Cell 153 2013 307 319
91. J.T. Witten, and J. Ule Understanding splicing regulation through RNA splicing maps Trends Genet. 27 2011 89 97
92. M.C. Wollerton, C. Gooding, E.J. Wagner, M.A. Garcia-Blanco, and C.W. Smith Autoregulation of polypyrimidine tract binding protein by alternative splicing leading to nonsense-mediated decay Mol. Cell 13 2004 91 100
93. Y. Xue, K. Ouyang, J. Huang, Y. Zhou, H. Ouyang, H. Li, G. Wang, Q. Wu, C. Wei, and Y. Bi Direct conversion of fibroblasts to neurons by reprogramming PTB-regulated microRNA circuits Cell 152 2013 82 96
94. Y.Y. Yang, G.L. Yin, and R.B. Darnell The neuronal RNA-binding protein Nova-2 is implicated as the autoantigen targeted in POMA patients with dementia Proc. Natl. Acad. Sci. USA 95 1998 13254 13259
95. K. Yoshida, M. Sanada, Y. Shiraishi, D. Nowak, Y. Nagata, R. Yamamoto, Y. Sato, A. Sato-Otsubo, A. Kon, and M. Nagasaki Frequent pathway mutations of splicing machinery in myelodysplasia Nature 478 2011 64 69
96. R.A. Young Control of the embryonic stem cell state Cell 144 2011 940 954
97. D.J. Young, A. Stoddart, J. Nakitandwe, S.C. Chen, Z. Qian, J.R. Downing, and M.M. Le Beau Knockdown of Hnrnpa0, a del(5q) gene, alters myeloid cell fate in murine cells through regulation of AU-rich transcripts Haematologica 99 2014 1032 1040
98. C. Zhang, Z. Zhang, J. Castle, S. Sun, J. Johnson, A.R. Krainer, and M.Q. Zhang Defining the regulatory network of the tissue-specific splicing factors Fox-1 and Fox-2 Genes Dev. 22 2008 2550 2563
99. C. Zhang, M.A. Frias, A. Mele, M. Ruggiu, T. Eom, C.B. Marney, H. Wang, D.D. Licatalosi, J.J. Fak, and R.B. Darnell Integrative modeling defines the Nova splicing-regulatory network and its combinatorial controls Science 329 2010 439 443
100. S. Zhou, Y. Yang, M.J. Scott, A. Pannuti, K.C. Fehr, A. Eisen, E.V. Koonin, D.L. Fouts, R. Wrightsman, and J.E. Manning Male-specific lethal 2, a dosage compensation gene of Drosophila, undergoes sex-specific regulation and encodes a protein with a RING finger and a metallothionein-like cysteine cluster EMBO J. 14 1995 2884 2895