Induced transcription and stability of CELF2 mRNA drives widespread alternative splicing during T-cell signaling

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 17, 2015, Pages E2139-E2148

  Mallory, Michael J ^a   Allon, Samuel J ^a   Qiu, Jinsong ^b   Gazzara, Matthew R ^a   Tapescu, Iulia ^a   Martinez, Nicole M ^a   Fu, Xiang Dong ^b   Lynch, Kristen W ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Alternative splicing; CELF2; mRNA stability; T cells; Thymic development

Indexed keywords

CELF2 PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LYMPHOID ENHANCER FACTOR 1; MESSENGER RNA; MICRORNA; RNA BINDING PROTEIN; TRANSCRIPTOME; UNCLASSIFIED DRUG; 3' UNTRANSLATED REGION; CELF PROTEIN; CELF2 PROTEIN, HUMAN; NERVE PROTEIN;

3' UNTRANSLATED REGION; ALTERNATIVE RNA SPLICING; ARTICLE; CELL DEATH; CONTROLLED STUDY; HUMAN; HUMAN CELL; JURKAT CELL LINE; MUSCLE CELL; NONSENSE MEDIATED MRNA DECAY; POLYADENYLATION; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; RNA PROCESSING; RNA STABILITY; RNA TRANSCRIPTION; SIGNAL TRANSDUCTION; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; THYMOCYTE; THYMUS; TRANSCRIPTION INITIATION; UPREGULATION; BIOSYNTHESIS; CYTOLOGY; GENETICS; METABOLISM; PHYSIOLOGY;

3' UNTRANSLATED REGIONS; ALTERNATIVE SPLICING; CELF PROTEINS; HUMANS; JURKAT CELLS; NERVE TISSUE PROTEINS; RNA STABILITY; RNA-BINDING PROTEINS; SIGNAL TRANSDUCTION; T-LYMPHOCYTES;

EID: 84928691633     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1423695112     Document Type: Article

References (68)

1. Smale ST (2012) Transcriptional regulation in the innate immune system. Curr Opin Immunol 24(1):51-57.
2. Carpenter S, Ricci EP, Mercier BC, Moore MJ, Fitzgerald KA (2014) Post-transcriptional regulation of gene expression in innate immunity. Nat Rev Immunol 14(6):361-376.
3. Moore MJ, Proudfoot NJ (2009) Pre-mRNA processing reaches back to transcription and ahead to translation. Cell 136(4):688-700.
4. Jangi M, Sharp PA (2014) Building robust transcriptomes with master splicing factors. Cell 159(3):487-498.
5. Fu XD, Ares M, Jr (2014) Context-dependent control of alternative splicing by RNA-binding proteins. Nat Rev Genet 15(10):689-701.
6. Singh RK, et al. (2014) Rbfox2-coordinated alternative splicing of Mef2d and Rock2 controls myoblast fusion during myogenesis. Mol Cell 55(4):592-603.
7. Raj B, et al. (2014) A global regulatory mechanism for activating an exon network required for neurogenesis. Mol Cell 56(1):90-103.
8. Ip JY, et al. (2007) Global analysis of alternative splicing during T-cell activation. RNA 13(4):563-572.
9. Lynch KW (2007) Regulation of alternative splicing by signal transduction pathways. Adv Exp Med Biol 623:161-174.
10. Martinez NM, et al. (2012) Alternative splicing networks regulated by signaling in human T cells. RNA 18(5):1029-1040.
11. Kalsotra A, Wang K, Li PF, Cooper TA (2010) MicroRNAs coordinate an alternative splicing network during mouse postnatal heart development. Genes Dev 24(7):653-658.
12. Zhou Z, et al. (2012) The Akt-SRPK-SR axis constitutes a major pathway in transducing EGF signaling to regulate alternative splicing in the nucleus. Mol Cell 47(3):422-433.
13. Warzecha CC, et al. (2010) An ESRP-regulated splicing programme is abrogated during the epithelial-mesenchymal transition. EMBO J 29(19):3286-3300.
14. Boutz PL, et al. (2007) A post-transcriptional regulatory switch in polypyrimidine tract-binding proteins reprograms alternative splicing in developing neurons. Genes Dev 21(13):1636-1652.
15. Kalsotra A, et al. (2008) A postnatal switch of CELF and MBNL proteins reprograms alternative splicing in the developing heart. Proc Natl Acad Sci USA 105(51):20333-20338.
16. Mallory MJ, et al. (2011) Signal- and development-dependent alternative splicing of LEF1 in T cells is controlled by CELF2. Mol Cell Biol 31(11):2184-2195.
17. Kane LP, Shapiro VS, Stokoe D, Weiss A (1999) Induction of NF-kappaB by the Akt/PKB kinase. Curr Biol 9(11):601-604.
18. Shapiro VS, Mollenauer MN, Greene WC, Weiss A (1996) c-rel regulation of IL-2 gene expression may be mediated through activation of AP-1. J Exp Med 184(5):1663-1669.
19. Yablonski D, Kane LP, Qian D, Weiss A (1998) A Nck-Pak1 signaling module is required for T-cell receptor-mediated activation of NFAT, but not of JNK. EMBO J 17(19):5647-5657.
20. Waelchli R, et al. (2006) Design and preparation of 2-benzamido-pyrimidines as inhibitors of IKK. Bioorg Med Chem Lett 16(1):108-112.
21. Pierce JW, et al. (1997) Novel inhibitors of cytokine-induced IkappaBalpha phosphorylation and endothelial cell adhesion molecule expression show anti-inflammatory effects in vivo. J Biol Chem 272(34):21096-21103.
22. Lee DH, Goldberg AL (1996) Selective inhibitors of the proteasome-dependent and vacuolar pathways of protein degradation in Saccharomyces cerevisiae. J Biol Chem 271(44):27280-27284.
23. Palombella VJ, Rando OJ, Goldberg AL, Maniatis T (1994) The ubiquitin-proteasome pathway is required for processing the NF-kappa B1 precursor protein and the activation of NF-kappa B. Cell 78(5):773-785.
24. Kunz J, Hall MN (1993) Cyclosporin A, FK506 and rapamycin: More than just immunosuppression. Trends Biochem Sci 18(9):334-338.
25. Favata MF, et al. (1998) Identification of a novel inhibitor of mitogen-activated protein kinase kinase. J Biol Chem 273(29):18623-18632.
26. Shin M, Yan C, Boyd D (2002) An inhibitor of c-jun aminoterminal kinase (SP600125) represses c-Jun activation, DNA-binding and PMA-inducible 92-kDa type IV collagenase expression. Biochim Biophys Acta 1589(3):311-316.
27. Grosveld GC (2009) Gamma-secretase inhibitors: Notch so bad. Nat Med 15(1):20-21.
28. Karam R, Wengrod J, Gardner LB, Wilkinson MF (2013) Regulation of nonsense-mediated mRNA decay: Implications for physiology and disease. Biochim Biophys Acta 1829(6-7):624-633.
29. Ni JZ, et al. (2007) Ultraconserved elements are associated with homeostatic control of splicing regulators by alternative splicing and nonsense-mediated decay. Genes Dev 21(6):708-718.
30. Prasanth KV, et al. (2005) Regulating gene expression through RNA nuclear retention. Cell 123(2):249-263.
31. Yap K, Makeyev EV (2013) Regulation of gene expression in mammalian nervous system through alternative pre-mRNA splicing coupled with RNA quality control mechanisms. Mol Cell Neurosci 56:420-428.
32. Pandya-Jones A, et al. (2013) Splicing kinetics and transcript release from the chromatin compartment limit the rate of Lipid A-induced gene expression. RNA 19(6):811-827.
33. Li H, Qiu J, Fu XD (2012) RASL-seq for massively parallel and quantitative analysis of gene expression. Curr Protoc Mol Biol, Chapter 4:Unit 4.13.1-9.
34. Martinez NM, Lynch KW (2013) Control of alternative splicing in immune responses: Many regulators, many predictions, much still to learn. Immunol Rev 253(1):216-236.
35. Dembowski JA, Grabowski PJ (2009) The CUGBP2 splicing factor regulates an ensemble of branchpoints from perimeter binding sites with implications for autoregulation. PLoS Genet 5(8):e1000595.
36. Saltzman AL, et al. (2008) Regulation of multiple core spliceosomal proteins by alternative splicing-coupled nonsense-mediated mRNA decay. Mol Cell Biol 28(13):4320-4330.
37. Rossbach O, et al. (2009) Auto- and cross-regulation of the hnRNP L proteins by alternative splicing. Mol Cell Biol 29(6):1442-1451.
38. Änkö ML, et al. (2012) The RNA-binding landscapes of two SR proteins reveal unique functions and binding to diverse RNA classes. Genome Biol 13(3):R17.
39. O'Dea E, Hoffmann A (2009) NF-κB signaling. Wiley Interdiscip Rev Syst Biol Med 1(1):107-115.
40. Voll RE, et al. (2000) NF-kappa B activation by the pre-T cell receptor serves as a selective survival signal in T lymphocyte development. Immunity 13(5):677-689.
41. Aifantis I, Gounari F, Scorrano L, Borowski C, von Boehmer H (2001) Constitutive pre-TCR signaling promotes differentiation through Ca2+ mobilization and activation of NF-kappaB and NFAT. Nat Immunol 2(5):403-409.
42. Cheadle C, et al. (2005) Control of gene expression during T cell activation: Alternate regulation of mRNA transcription and mRNA stability. BMC Genomics 6:75.
43. Blencowe B, Brenner S, Hughes T, Morris Q (2009) Post-transcriptional gene regulation: RNA-protein interactions, RNA processing, mRNA stability and localization. Pac Symp Biocomput 2009:545-548.
44. Pasquinelli AE (2012) MicroRNAs and their targets: Recognition, regulation and an emerging reciprocal relationship. Nat Rev Genet 13(4):271-282.
45. Dooley J, Linterman MA, Liston A (2013) MicroRNA regulation of T-cell development. Immunol Rev 253(1):53-64.
46. Braunschweig U, et al. (2014) Widespread intron retention in mammals functionally tunes transcriptomes. Genome Res 24(11):1774-1786.
47. Gudikote JP, Wilkinson MF (2002) T-cell receptor sequences that elicit strong downregulation of premature termination codon-bearing transcripts. EMBO J 21(1-2):125-134.
48. Reznik B, Lykke-Andersen J (2010) Regulated and quality-control mRNA turnover pathways in eukaryotes. Biochem Soc Trans 38(6):1506-1510.
49. Ladd AN (2013) CUG-BP, Elav-like family (CELF)-mediated alternative splicing regulation in the brain during health and disease. Mol Cell Neurosci 56:456-464.
50. Ladd AN, Charlet N, Cooper TA (2001) The CELF family of RNA binding proteins is implicated in cell-specific and developmentally regulated alternative splicing. Mol Cell Biol 21(4):1285-1296.
51. Lenardo MJ (2003) Molecular regulation of T lymphocyte homeostasis in the healthy and diseased immune system. Immunol Res 27(2-3):387-398.
52. Smith-Garvin JE, Koretzky GA, Jordan MS (2009) T cell activation. Annu Rev Immunol 27:591-619.
53. Huelga SC, et al. (2012) Integrative genome-wide analysis reveals cooperative regulation of alternative splicing by hnRNP proteins. Cell Reports 1(2):167-178.
54. Jangi M, Boutz PL, Paul P, Sharp PA (2014) Rbfox2 controls autoregulation in RNA-binding protein networks. Genes Dev 28(6):637-651.
55. Wang HY, et al. (1998) SRPK2: A differentially expressed SR protein-specific kinase involved in mediating the interaction and localization of pre-mRNA splicing factors in mammalian cells. J Cell Biol 140(4):737-750.
56. Zhou Z, Fu XD (2013) Regulation of splicing by SR proteins and SR protein-specific kinases. Chromosoma 122(3):191-207.
57. Zhong XY, Wang P, Han J, Rosenfeld MG, Fu XD (2009) SR proteins in vertical integration of gene expression from transcription to RNA processing to translation. Mol Cell 35(1):1-10.
58. Adamson P, Etienne S, Couraud PO, Calder V, Greenwood J (1999) Lymphocyte migration through brain endothelial cell monolayers involves signaling through endothelial ICAM-1 via a rho-dependent pathway. J Immunol 162(5):2964-2973.
59. Gattazzo C, et al. (2014) Cortactin, another player in the Lyn signaling pathway, is over-expressed and alternatively spliced in leukemic cells from patients with B-cell chronic lymphocytic leukemia. Haematologica 99(6):1069-1077.
60. Kirkbride KC, Sung BH, Sinha S, Weaver AM (2011) Cortactin: A multifunctional regulator of cellular invasiveness. Cell Adhes Migr 5(2):187-198.
61. Chen L, et al. (2012) OPA1 mutation and late-onset cardiomyopathy: mitochondrial dysfunction and mtDNA instability. J Am Heart Assoc 1(5):e003012.
62. Nicolas M, Hassan BA (2014) Amyloid precursor protein and neural development. Development 141(13):2543-2548.
63. Deng H, Gao K, Jankovic J (2014) The role of FUS gene variants in neurodegenerative diseases. Nat Rev Neurol 10(6):337-348.
64. Lynch KW, Weiss A (2000) A model system for activation-induced alternative splicing of CD45 pre-mRNA in T cells implicates protein kinase C and Ras. Mol Cell Biol 20(1):70-80.
65. Bresson SM, Conrad NK (2013) The human nuclear poly(a)-binding protein promotes RNA hyperadenylation and decay. PLoS Genet 9(10):e1003893.
66. Rothrock C, Cannon B, Hahm B, Lynch KW (2003) A conserved signal-responsive sequence mediates activation-induced alternative splicing of CD45. Mol Cell 12(5):1317-1324.
67. Heyd F, Lynch KW (2010) Phosphorylation-dependent regulation of PSF by GSK3 controls CD45 alternative splicing. Mol Cell 40(1):126-137.
68. Landt SG, et al. (2012) ChIP-seq guidelines and practices of the ENCODE and modENCODE consortia. Genome Res 22(9):1813-1831.