Artículo

Estamos trabajando para incorporar este artículo al repositorio
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor

Abstract:

Alternative splicing (AS) greatly expands the coding capacities of genomes by allowing the generation of multiple mature mRNAs from a limited number of genes. Although the massive switch in AS profiles that often accompanies variations in gene expression patterns occurring during cell differentiation has been characterized for a variety of models, their causes and mechanisms remain largely unknown. Here, we integrate foundational and recent studies indicating the AS switches that govern the processes of cell fate determination. We include some distinct AS events in pluripotent cells and somatic reprogramming and discuss new progresses on alternative isoform expression in adipogenesis, myogenic differentiation and stimulation of immune cells. Finally, we cover novel insights on AS mechanisms during neuronal differentiation, paying special attention to the role of chromatin structure. © 2017 WILEY Periodicals, Inc.

Registro:

Documento: Artículo
Título:Alternative splicing switches: Important players in cell differentiation
Autor:Fiszbein, A.; Kornblihtt, A.R.
Filiación:Instituto de Fisiología, Biología Molecular y Neurociencias (IFIBYNE-UBA-CONICET) and Departamento de Fisiología, Biología Molecular y Celular, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Ciudad Universitaria, Buenos Aires, C1428EHA, Argentina
Palabras clave:alternative splicing; cell differentiation; chromatin structure; neuronal differentiation; RNA binding proteins; spliceosome; splicing factors; RNA; adipogenesis; alternative RNA splicing; cell differentiation; chromatin structure; embryonic stem cell; gene expression; human; immunocompetent cell; immunostimulation; muscle development; nerve cell differentiation; nuclear reprogramming; pluripotent stem cell; regulatory mechanism; Review; animal; cell differentiation; genetics; Alternative Splicing; Animals; Cell Differentiation; Humans
Año:2017
Volumen:39
Número:6
DOI: http://dx.doi.org/10.1002/bies.201600157
Título revista:BioEssays
Título revista abreviado:BioEssays
ISSN:02659247
CODEN:BIOEE
CAS:RNA, 63231-63-0
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_02659247_v39_n6_p_Fiszbein

Referencias:

  • Reik, W., Stability and flexibility of epigenetic gene regulation in mammalian development (2007) Nature, 447, pp. 425-432
  • Goldberg, A.D., Allis, C.D., Bernstein, E., Epigenetics: a landscape takes shape (2007) Cell, 128, pp. 635-638
  • Morgan, H.D., Santos, F., Green, K., Dean, W., Epigenetic reprogramming in mammals (2005) Hum Mol Genet, 14, pp. R47-58
  • Bird, A., DNA methylation patterns and epigenetic memory (2002) Genes Dev, 16, pp. 6-21
  • Monk, M., Boubelik, M., Lehnert, S., Temporal and regional changes in DNA methylation in the embryonic, extraembryonic and germ cell lineages during mouse embryo development (1987) Development, 99, pp. 371-382
  • Kafri, T., Ariel, M., Brandeis, M., Shemer, R., Developmental pattern of gene-specific DNA methylation in the mouse embryo and germ line (1992) Genes Dev, 6, pp. 705-714
  • Boyer, L.A., Plath, K., Zeitlinger, J., Brambrink, T., Polycomb complexes repress developmental regulators in murine embryonic stem cells (2006) Nature, 441, pp. 349-353
  • Takahashi, K., Yamanaka, S., Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors (2006) Cell, 126, pp. 663-676
  • Burge, C.S., Tuschl, T., Sharp, P.A., Splicing of precursors to mRNAs by the spliceosomes (1999) The RNA World, pp. 525-560. , In, Second Edition. New York Cold Spring Harbor Laboratory Press. p
  • Li, Q., Lee, J.-A., Black, D.L., Neuronal regulation of alternative pre-mRNA splicing (2007) Nat Rev Neurosci, 8, pp. 819-831
  • Black, D.L., Protein diversity from alternative splicing: a challenge for bioinformatics and post-genome biology (2000) Cell, 103, pp. 367-370
  • Castle, J.C., Zhang, C., Shah, J.K., Kulkarni, A.V., Expression of 24,426 human alternative splicing events and predicted cis regulation in 48 tissues and cell lines (2008) Nat Genet, 40, pp. 1416-1425
  • Barbosa-Morais, N.L., Irimia, M., Pan, Q., Xiong, H.Y., The evolutionary landscape of alternative splicing in vertebrate species (2012) Science, 338, pp. 1587-1593
  • Merkin, J., Russell, C., Chen, P., Burge, C.B., Evolutionary dynamics of gene and isoform regulation in mammalian tissues (2012) Science, 338, pp. 1593-1599
  • Cieply, B., Carstens, R.P., Functional roles of alternative splicing factors in human disease (2015) Wiley Interdiscip Rev RNA, 6, pp. 311-326
  • Wagner, S.D., Struck, A.J., Gupta, R., Farnsworth, D.R., Dose-dependent regulation of alternative splicing by MBNL proteins reveals biomarkers for myotonic dystrophy (2016) PLoS Genet, 12
  • Pritsker, M., Doniger, T.T., Kramer, L.C., Westcot, S.E., Diversification of stem cell molecular repertoire by alternative splicing (2005) Proc Natl Acad Sci USA, 102, pp. 14290-14295
  • Wu, J.Q., Habegger, L., Noisa, P., Szekely, A., Dynamic transcriptomes during neural differentiation of human embryonic stem cells revealed by short, long, and paired-end sequencing (2010) Proc Natl Acad Sci USA, 107, pp. 5254-5259
  • Salomonis, N., Schlieve, C.R., Pereira, L., Wahlquist, C., Alternative splicing regulates mouse embryonic stem cell pluripotency and differentiation (2010) Proc Natl Acad Sci USA, 107, pp. 10514-10519
  • Yeo, G.W., Xu, X., Liang, T.Y., Muotri, A.R., Alternative splicing events identified in human embryonic stem cells and neural progenitors (2007) PLoS Comput Biol, 3, pp. 1951-1967
  • Boyer, L.A., Lee, T.I., Cole, M.F., Johnstone, S.E., Core transcriptional regulatory circuitry in human embryonic stem cells (2005) Cell, 122, pp. 947-956
  • Loh, Y.-H., Wu, Q., Chew, J.-L., Vega, V.B., The Oct4 and Nanog transcription network regulates pluripotency in mouse embryonic stem cells (2006) Nat Genet, 38, pp. 431-440
  • Azuara, V., Perry, P., Sauer, S., Spivakov, M., Chromatin signatures of pluripotent cell lines (2006) Nat Cell Biol, 8, pp. 532-538
  • Bernstein, B.E., Mikkelsen, T.S., Xie, X., Kamal, M., A bivalent chromatin structure marks key developmental genes in embryonic stem cells (2006) Cell, 125, pp. 315-326
  • Guenther, M.G., Levine, S.S., Boyer, L.A., Jaenisch, R., A chromatin landmark and transcription initiation at most promoters in human cells (2007) Cell, 130, pp. 77-88
  • Kim, J., Chu, J., Shen, X., Wang, J., An extended transcriptional network for pluripotency of embryonic stem cells (2008) Cell, 132, pp. 1049-1061
  • Mikkelsen, T.S., Ku, M., Jaffe, D.B., Issac, B., Genome-wide maps of chromatin state in pluripotent and lineage-committed cells (2007) Nature, 448, pp. 553-560
  • Revil, T., Gaffney, D., Dias, C., Majewski, J., Alternative splicing is frequent during early embryonic development in mouse (2010) BMC Genomics, 11, p. 399
  • Gabut, M., Samavarchi-Tehrani, P., Wang, X., Slobodeniuc, V., An alternative splicing switch regulates embryonic stem cell pluripotency and reprogramming (2011) Cell, 147, pp. 132-146
  • Han, H., Irimia, M., Ross, P.J., Sung, H.-K., MBNL proteins repress ES-cell-specific alternative splicing and reprogramming (2013) Nature, 498, pp. 241-245
  • Aaronson, Y., Meshorer, E., Stem cells: regulation by alternative splicing (2013) Nature, 498, pp. 176-177
  • Zeineddine, D., Hammoud, A.A., Mortada, M., Boeuf, H., The Oct4 protein: more than a magic stemness marker (2014) Am J Stem Cells, 3, pp. 74-82
  • Niwa, H., Miyazaki, J., Smith, A.G., Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells (2000) Nat Genet, 24, pp. 372-376
  • Tahmasebi, S., Jafarnejad, S.M., Tam, I.S., Gonatopoulos-Pournatzis, T., Control of embryonic stem cell self-renewal and differentiation via coordinated alternative splicing and translation of YY2 (2016) Proc Natl Acad Sci USA, 113, pp. 12360-12367
  • Wang, X., Dai, J., Concise review: isoforms of OCT4 contribute to the confusing diversity in stem cell biology (2010) Stem Cells, 28, pp. 885-893
  • Poursani, E.M., Soltani, B.M., Mowla, S.J., Differential expression of OCT4 pseudogenes in pluripotent and tumor cell lines (2016) Cell J, 18, pp. 28-36
  • Ohta, S., Nishida, E., Yamanaka, S., Yamamoto, T., Global splicing pattern reversion during somatic cell reprogramming (2013) Cell Rep, 5, pp. 357-366
  • Venables, J.P., Lapasset, L., Gadea, G., Fort, P., MBNL1 and RBFOX2 cooperate to establish a splicing programme involved in pluripotent stem cell differentiation (2013) Nat Commun, 4, p. 2480
  • Cieply, B., Park, J.W., Nakauka-Ddamba, A., Bebee, T.W., Multiphasic and dynamic changes in alternative splicing during induction of pluripotency are coordinated by numerous RNA-binding proteins (2016) Cell Rep, 15, pp. 247-255
  • Ma, Q., Fan, J., Wang, J., Yang, S., High levels of chorionic gonadotrophin attenuate insulin sensitivity and promote inflammation in adipocytes (2015) J Mol Endocrinol, 54, pp. 161-170
  • Mei, B., Zhao, L., Chen, L., Sul, H.S., Only the large soluble form of preadipocyte factor-1 (Pref-1), but not the small soluble and membrane forms, inhibits adipocyte differentiation: role of alternative splicing (2002) Biochem J, 364, pp. 137-144
  • Entingh, A.J., Taniguchi, C.M., Kahn, C.R., Bi-directional regulation of brown fat adipogenesis by the insulin receptor (2003) J Biol Chem, 278, pp. 33377-33383
  • Huot, M.-É., Vogel, G., Zabarauskas, A., Ngo, C.T.A., The sam68 STAR RNA-Binding protein regulates mTOR alternative splicing during adipogenesis (2012) Mol Cell, 46, pp. 187-199
  • Zhao, X., Yang, Y.Y.-G., Sun, B.-F., Shi, Y., FTO-dependent demethylation of N6-methyladenosine regulates mRNA splicing and is required for adipogenesis (2014) Cell Res, 24, pp. 1403-1419
  • Lin, J.C., Impacts of alternative splicing events on the differentiation of adipocytes (2015) Int J Mol Sci, 16, pp. 22169-22189
  • Bland, C.S., Wang, E.T., Vu, A., David, M.P., Global regulation of alternative splicing during myogenic differentiation (2010) Nucleic Acids Res, 38, pp. 7651-7664
  • Runfola, V., Sebastian, S., Dilworth, F.J., Gabellini, D., Rbfox proteins regulate tissue-specific alternative splicing of Mef2D required for muscle differentiation (2015) J Cell Sci, 128, pp. 631-637
  • Singh, R.K., Xia, Z., Bland, C.S., Kalsotra, A., Rbfox2-coordinated alternative splicing of Mef2d and Rock2 controls myoblast fusion during myogenesis (2014) Mol Cell, 55, pp. 592-603
  • Cardinali, B., Cappella, M., Provenzano, C., Garcia-Manteiga, J.M., MicroRNA-222 regulates muscle alternative splicing through Rbm24 during differentiation of skeletal muscle cells (2016) Cell Death Dis, 7
  • Wang, E.T., Ward, A.J., Cherone, J.M., Giudice, J., Antagonistic regulation of mRNA expression and splicing by CELF and MBNL proteins (2015) Genome Res, 25, pp. 858-871
  • Charlet-B, N., Savkur, R.S., Singh, G., Philips, A.V., Loss of the muscle-specific chloride channel in type 1 myotonic dystrophy due to misregulated alternative splicing (2002) Mol Cell, 10, pp. 45-53
  • Savkur, R.S., Philips, A.V., Cooper, T.A., Aberrant regulation of insulin receptor alternative splicing is associated with insulin resistance in myotonic dystrophy (2001) Nat Genet, 29, pp. 40-47
  • Fugier, C., Klein, A.F., Hammer, C., Vassilopoulos, S., Misregulated alternative splicing of BIN1 is associated with T tubule alterations and muscle weakness in myotonic dystrophy (2011) Nat Med, 17, pp. 720-725
  • Martinez, N.M., Lynch, K.W., Control of alternative splicing in immune responses: many regulators, many predictions, much still to learn (2013) Immunol Rev, 253, pp. 216-236
  • Martinez, N.M., Pan, Q., Cole, B.S., Yarosh, C.A., Alternative splicing networks regulated by signaling in human T cells (2012) RNA, 18, pp. 1029-1040
  • Ajith, S., Gazzara, M.R., Cole, B.S., Shankarling, G., Position-dependent activity of CELF2 in the regulation of splicing and implications for signal-responsive regulation in T cells (2016) RNA Biol, 13, pp. 569-581
  • Mallory, M.J., Allon, S.J., Qiu, J., Gazzara, M.R., Induced transcription and stability of CELF2 mRNA drives widespread alternative splicing during T-cell signaling (2015) Proc Natl Acad Sci USA, 112, pp. E2139-E2148
  • Cole, B.S., Tapescu, I., Allon, S.J., Mallory, M.J., Global analysis of physical and functional RNA targets of hnRNP L reveals distinct sequence and epigenetic features of repressed and enhanced exons (2015) RNA, 21, pp. 2053-2066
  • Ni, T., Yang, W., Han, M., Zhang, Y., Global intron retention mediated gene regulation during CD4+ T cell activation (2016) Nucleic Acids Res, 44, pp. 6817-6829
  • Wong, J.J.L., Ritchie, W., Ebner, O.A., Selbach, M., Orchestrated intron retention regulates normal granulocyte differentiation (2013) Cell, 154, pp. 583-595
  • Vuong, C.K., Black, D.L., Zheng, S., The neurogenetics of alternative splicing (2016) Nat Rev Neurosci, 17, pp. 265-281
  • Rosenfeld, M.G., Mermod, J.-J., Amara, S.G., Swanson, L.W., Production of a novel neuropeptide encoded by the calcitonin gene via tissue-specific RNA processing (1983) Nature, 304, pp. 129-135
  • Suzuki, H., Osaki, K., Sano, K., Alam, A.H.M.K., Comprehensive analysis of alternative splicing and functionality in neuronal differentiation of P19 cells (2011) PLoS ONE, 6
  • Alam, S., Phan, H.T., Okazaki, M., Takagi, M., Computational extraction of a neural molecular network through alternative splicing (2014) BMC Res Notes, 7, p. 934
  • Tarn, W.-Y., Kuo, H.-C., Yu, H.-I., Liu, S.-W., RBM4 promotes neuronal differentiation and neurite outgrowth via modulating Numb isoform expression (2016) Mol Biol Cell, 4, pp. 1-6
  • Kim, K.K., Nam, J., Mukouyama, Y.-S., Kawamoto, S., Rbfox3-regulated alternative splicing of Numb promotes neuronal differentiation during development (2013) J Cell Biol, 200, pp. 443-458
  • Xue, Y., Ouyang, K., Huang, J., Zhou, Y., Direct conversion of fibroblasts to neurons by reprogramming PTB-regulated MicroRNA circuits (2013) Cell, 152, pp. 82-96
  • Licatalosi, D.D., Yano, M., Fak, J.J., Mele, A., Ptbp2 represses adult-specific splicing to regulate the generation of neuronal precursors in the embryonic brain (2012) Genes Dev, 26, pp. 1626-1642
  • Ule, J., Stefani, G., Mele, A., Ruggiu, M., An RNA map predicting Nova-dependent splicing regulation (2006) Nature, 444, pp. 580-586
  • Ince-Dunn, G., Okano, H.J., Jensen, K.B., Park, W.Y., Neuronal Elav-Like (Hu) proteins regulate RNA splicing and abundance to control glutamate levels and neuronal excitability (2012) Neuron, 75, pp. 1067-1079
  • Pandya-Jones, A., Black, D.L., Co-transcriptional splicing of constitutive and alternative exons (2009) RNA, 15, pp. 1896-1908
  • Chong, J.A., Tapia-Ramirez, J., Kim, S., Toledo-Aral, J.J., REST: a mammalian silencer protein that restricts sodium channel gene expression to neurons (1995) Cell, 80, pp. 949-957
  • Schoenherr, C.J., Anderson, D.J., The neuron-restrictive silencer factor (NRSF): a coordinate repressor of multiple neuron-specific genes (1995) Science, 267, pp. 1360-1363
  • Shimojo, M., Paquette, A.J., Anderson, D.J., Hersh, L.B., Protein kinase A regulates cholinergic gene expression in PC12 cells: rEST4 silences the silencing activity of neuron-restrictive silencer factor/REST (1999) Mol Cell Biol, 19, pp. 6788-6795
  • Raj, B., O'Hanlon, D., Vessey, J.P., Pan, Q., Cross-regulation between an alternative splicing activator and a transcription repressor controls neurogenesis (2011) Mol Cell, 43, pp. 843-850
  • Fiszbein, A., Schor, I.E., Kornblihtt, A.R., Fundamentals of NCAM expression, function, and regulation of alternative splicing in neuronal differentiation (2015) Neural Surface Antigens, pp. 131-140. , In, Pruszak J, ed;, London, San Diego, Waltham, Oxford, Academic Press, Elsevier, p
  • Doherty, P., Rimon, G., Mann, D.A., Walsh, F.S., Alternative splicing of the cytoplasmic domain of neural cell adhesion molecule alters its ability to act as a substrate for neurite outgrowth (1992) J Neurochem, 58, pp. 2338-2341
  • Persohn, E., Schachner, M., Immunohistological localization of the neural adhesion molecules L1 and N-CAM in the developing hippocampus of the mouse (1990) J Neurocytol, 19, pp. 807-819
  • Schor, I.E., Rascovan, N., Pelisch, F., Alló, M., Neuronal cell depolarization induces intragenic chromatin modifications affecting NCAM alternative splicing (2009) Proc Natl Acad Sci USA, 106, pp. 4325-4330
  • Schor, I.E., Fiszbein, A., Petrillo, E., Kornblihtt, A.R., Intragenic epigenetic changes modulate NCAM alternative splicing in neuronal differentiation (2013) EMBO J, 32, pp. 2264-2274
  • Laurent, B., Ruitu, L., Murn, J., Hempel, K., A specific LSD1/KDM1A isoform regulates neuronal differentiation through H3K9 demethylation (2015) Mol Cell, 57, pp. 957-970
  • Fiszbein, A., Giono, L.E., Quaglino, A., Berardino, B.G., Alternative splicing of G9a regulates neuronal differentiation (2016) Cell Rep, 14, pp. 2797-2808

Citas:

---------- APA ----------
Fiszbein, A. & Kornblihtt, A.R. (2017) . Alternative splicing switches: Important players in cell differentiation. BioEssays, 39(6).
http://dx.doi.org/10.1002/bies.201600157
---------- CHICAGO ----------
Fiszbein, A., Kornblihtt, A.R. "Alternative splicing switches: Important players in cell differentiation" . BioEssays 39, no. 6 (2017).
http://dx.doi.org/10.1002/bies.201600157
---------- MLA ----------
Fiszbein, A., Kornblihtt, A.R. "Alternative splicing switches: Important players in cell differentiation" . BioEssays, vol. 39, no. 6, 2017.
http://dx.doi.org/10.1002/bies.201600157
---------- VANCOUVER ----------
Fiszbein, A., Kornblihtt, A.R. Alternative splicing switches: Important players in cell differentiation. BioEssays. 2017;39(6).
http://dx.doi.org/10.1002/bies.201600157