Decrease in hnRNP A/B expression during erythropoiesis mediates a pre-mRNA splicing switch

EMBO Journal

Volumn 21, Issue 22, 2002, Pages 6195-6204

  Hou, Victor C ^a   Lersch, Robert ^a   Gee, Sherry L ^a   Ponthier, Julie L ^a   Lo, Annie J ^a   Wu, Michael ^b   Turck, Chris W ^c   Koury, Mark ^d   Krainer, Adrian R ^e   Mayeda, Akila ^f   Conboy, John G ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b University of California Berkeley   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d VANDERBILT UNIVERSITY   (United States)

^e Howard Hughes Medical Institute Cold Spring Harbor Laboratory Cold Spring Harbor   (United States)

^f UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

Author keywords

Alternative splicing; Exonic splicing silencer; hnRNP A and B; Protein 4.1R

Indexed keywords

ERYTHROCYTE BAND 4.1 PROTEIN; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN A; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN B; MESSENGER RNA PRECURSOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; ERYTHROBLAST; ERYTHROPOIESIS; EXON; GENE REPRESSION; GENE SEQUENCE; GENE SILENCING; GENETIC RECOMBINATION; HUMAN; HUMAN CELL; INTRON; MOUSE; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; RNA SPLICING; SILENCER GENE;

ALTERNATIVE SPLICING; ANIMALS; BASE SEQUENCE; CONSENSUS SEQUENCE; CYTOSKELETAL PROTEINS; ERYTHROID PROGENITOR CELLS; ERYTHROPOIESIS; EXONS; GENE EXPRESSION REGULATION; GENE SILENCING; HELA CELLS; HETEROGENEOUS-NUCLEAR RIBONUCLEOPROTEIN GROUP A-B; HUMANS; INTRONS; MEMBRANE PROTEINS; MICE; MOLECULAR SEQUENCE DATA; MUTAGENESIS; NEUROPEPTIDES; PROTEIN BINDING; PROTEINS; REGULATORY SEQUENCES, NUCLEIC ACID; RNA PRECURSORS; RNA-BINDING PROTEINS; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, NUCLEIC ACID; SPECIES SPECIFICITY; TRANSFECTION; VERTEBRATES; XENOPUS LAEVIS;

ANIMALIA;

EID: 18744384006     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/cdf625     Document Type: Article

References (65)

1. Amendt, B.A., Si, Z.H. and Stoltzfus, C.M. (1995) Presence of exon splicing silencers within human immunodeficiency virus type 1 tat exon 2 and tat-rev exon 3: Evidence for inhibition mediated by cellular factors. Mol. Cell. Biol., 15, 4606-4615.
2. Ashiya, M. and Grabowski, P.J. (1997) A neuron-specific splicing switch mediated by an array of pre-mRNA repressor sites: Evidence of a regulatory role for the polypyrimidine tract binding protein and a brain-specific PTB counterpart. RNA, 3, 996-1015.
3. Bagga, P.S., Ford, L.P., Chen, F. and Wilusz, J. (1995) The G-rich auxiliary downstream element has distinct sequence and position requirements and mediates efficient 3′ end pre-mRNA processing through a trans-acting factor. Nucleic Acids Res., 23, 1625-1631.
4. Bai, Y., Lee, D., Yu, T. and Chasin, L.A. (1999) Control of 3′ splice site choice in vivo by ASF/SF2 and hnRNP A1. Nucleic Acids Res., 27, 1126-1134.
5. Baklouti, F., Huang, S.C., Vulliamy, T.J., Delaunay, J. and Benz, E.J., Jr (1997) Organization of the human protein 4.1 genomic locus: New insights into the tissue-specific alternative splicing of the pre-mRNA. Genomics, 39, 289-302.
6. Berget, S.M. (1995) Exon recognition in vertebrate splicing. J. Biol. Chem., 270, 2411-2414.
7. Bilodeau, P.S., Domsic, J.K., Mayeda, A., Krainer, A.R. and Stoltzfus, C.M. (2001) RNA splicing at human immunodeficiency virus type 1 3′ splice site A2 is regulated by binding of hnRNP A/B proteins to an exonic splicing silencer element. J. Virol., 75, 8487-8497.
8. Blanchette, M. and Chabot, B. (1999) Modulation of exon skipping by high-affinity hnRNP A1-binding sites and by intron elements that repress splice site utilization. EMBO J., 18, 1939-1952.
9. Caceres, J.F., Stamm, S., Helfman, D.M. and Krainer, A.R. (1994) Regulation of alternative splicing in vivo by overexpression of antagonistic splicing factors. Science, 265, 1706-1709.
10. Caputi, M., Mayeda, A., Krainer, A.R. and Zahler, A.M. (1999) hnRNP A/ B proteins are required for inhibition of HIV-1 pre-mRNA splicing. EMBO J., 18, 4060-4067.
11. Chabot, B. (1996) Directing alternative splicing: Cast and scenarios. Trends Genet., 12, 472-478.
12. Chan, R.C. and Black, D.L. (1997) The polypyrimidine tract binding protein binds upstream of neural cell-specific c-src exon N1 to repress the splicing of the intron downstream. Mol. Cell. Biol., 17, 4667-4676.
13. 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 hematopoiesis. J. Clin. Invest., 91, 329-338.
14. Conboy, J. (1999) The role of alternative pre-mRNA splicing in regulating the structure and function of skeletal protein 4.1. Proc. Soc. Exp. Biol. Med., 220, 73-78.
15. Conboy, J.G., Chan, J., Chasis, J.A., Kan, Y.W. and Mohandas, N. (1991a) Tissue- and development-specific alternative RNA splicing regulates expression of multiple isoforms of erythroid membrane protein 4.1. J. Biol. Chem., 266, 8273-8280.
16. Conboy, J.G., Shitamoto, R., Parra, M., Winardi, R., Kabra, A., Smith, J. and Mohandas, N. (1991b) Hereditary elliptocytosis due to both qualitative and quantitative defects in membrane skeletal protein 4.1. Blood, 78, 2438-2443.
17. Deguillien, M., Huang, S.C., Moriniere, M., Dreumont, N., Benz, E.J., Jr and Baklouti, F. (2001) Multiple cis elements regulate an alternative splicing event at 4.1R pre-mRNA during erythroid differentiation. Blood, 98, 3809-3816.
18. Del Gatto, F. and Breathnach, R. (1995) Exon and intron sequences, respectively, repress and activate splicing of a fibroblast growth factor receptor 2 alternative exon. Mol. Cell. Biol., 15, 4825-4834.
19. Del Gatto, F., Gesnel, M.C. and Breathnach, R. (1996) The exon sequence TAGG can inhibit splicing. Nucleic Acids Res., 24, 2017-2021.
20. Del Gatto-Konczak, F., Olive, M., Gesnel, M.C. and Breathnach, R. (1999) hnRNP A1 recruited to an exon in vivo can function as an exon splicing silencer. Mol. Cell. Biol., 19, 251-260.
21. Ding, J., Hayashi, M.K., Zhang, Y., Manche, L., Krainer, A.R. and Xu, R.M. (1999) Crystal structure of the two-RRM domain of hnRNP A1 (UP1) complexed with single-stranded telomeric DNA. Genes Dev., 13, 1102-1115.
22. 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.
23. Discher, D.E., Winardi, R., Schischmanoff, P.O., Parra, M., Conboy, J.G. and Mohandas, N. (1995) Mechanochemistry of protein 4.1's spectrin-actin-binding domain: Ternary complex interactions, membrane binding, network integration, structural strengthening. J. Cell Biol., 130, 897-907.
24. Eng, Y., McCormack, A.L. and Yates, J.R., III (1994) An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database. J. Am. Soc. Mass Spectrom., 5, 976-989.
25. Fu, X.D., Mayeda, A., Maniatis, T. and Krainer, A.R. (1992) General splicing factors SF2 and SC35 have equivalent activities in vitro and both affect alternative 5′ and 3′ splice site selection. Proc. Natl Acad. Sci. USA, 89, 11224-11228.
26. Gascard, P., Nunomura, W., Lee, G., Walensky, L., Krauss, S.W., Takakuwa, Y., Chasis, J.A., Mohandas, M. and Conboy, J.G. (1999) Deciphering the nuclear import pathway for the cytoskeletal protein 4.1R. Mol. Biol. Cell, 10, 1783-1798.
27. Gee, S.L., Parra, M., Willig, T., Hou, V.C., Chan, N., Wu, M. and Conboy, J.G. (1998) Alternative splicing of protein 4.1 exon 16 is regulated in part by downstream intron elements. Blood, 92, Suppl. 1, 5a.
28. Gee, S.L., Aoyagi, K., Lersch, R., Hou, V., Wu, M. and Conboy, J.G. (2000) Alternative splicing of protein 4.1R exon 16: Ordered excision of flanking introns ensures proper splice site choice. Blood, 95, 692-699.
29. Graham, I.R., Hamshere, M. and Eperon, I.C. (1992) Alternative splicing of a human α-tropomyosin muscle-specific exon: Identification of determining sequences. Mol. Cell. Biol., 12, 3872-3882.
30. Hellman, U., Wernstedt, C., Gonez, J. and Heldin, C.H. (1995) Improvement of an in-gel digestion procedure for the micropreparation of internal protein fragments for amino acid sequencing. Anal. Biochem., 224, 451-455.
31. Hertel, K.J., Lynch, K.W. and Maniatis, T. (1997) Common themes in the function of transcription and splicing enhancers. Curr. Opin. Cell Biol., 9, 350-357.
32. Horne, W.C., Huang, S.C., Becker, P.S., Tang, T.K. and Benz, E.J.J. (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.
33. Huang, J.-P., Tang, C.-J., Kou, G.-H., Marchesi, T., Benz, E.J., Jr and Tang, T.K. (1993) Genomic structure of the locus encoding protein 4.1. Structural basis for complex combinational patterns of tissue-specific alternative RNA splicing. J. Biol. Chem., 268, 3758-3766.
34. Kan, J.L. and Green, M.R. (1999) Pre-mRNA splicing of IgM exons M1 and M2 is directed by a juxtaposed splicing enhancer and inhibitor. Genes Dev., 13, 462-471.
35. Konig, H., Ponta, H. and Herrlich, P. (1998) Coupling of signal transduction to alternative pre-mRNA splicing by a composite splice regulator. EMBO J., 17, 2904-2913.
36. Koury, M.J., Sawyer, S.T. and Bondurant, M.C. (1984) Splenic erythroblasts in anemia-inducing Friend disease: A source of cells for studies of erythropoietin-mediated differentiation. J. Cell. Physiol., 121, 526-532.
37. Koury, S.T., Koury, M.J. and Bondurant, M.C. (1989) Cytoskeletal distribution and function during the maturation and enucleation of mammalian erythroblasts. J. Cell Biol., 109, 3005-3013.
38. Lander, E.S. et al. (2001) Initial sequencing and analysis of the human genome. Nature, 409, 860-921.
39. Liu, H.X., Zhang, M. and Krainer, A.R. (1998) Identification of functional exonic splicing enhancer motifs recognized by individual SR proteins. Genes Dev., 12, 1998-2012.
40. Luque, C.M., Lallena, M.J., Alonso, M.A. and Correas, I. (1998) An alternative domain determines nuclear localization in multifunctional protein 4.1. J. Biol. Chem., 273, 11643-11649.
41. Lynch, K.W. and Maniatis, T. (1995) Synergistic interactions between two distinct elements of a regulated splicing enhancer. Genes Dev., 9, 284-293.
42. Matter, N., Marx, M., Weg-Remers, S., Ponta, H., Herrlich, P. and Konig, H. (2000) Heterogeneous ribonucleoprotein A1 is part of an exon-specific splice-silencing complex controlled by oncogenic signaling pathways. J. Biol. Chem., 275, 35353-35360.
43. Mayeda, A. and Krainer, A.R. (1992) Regulation of alternative pre-mRNA splicing by hnRNP A1 and splicing factor SF2. Cell, 68, 365-375.
44. Mayeda, A. and Krainer, A.R. (1999a) Mammalian in vitro splicing assays. Methods Mol. Biol., 118, 315-321.
45. Mayeda, A. and Krainer, A.R. (1999b) Preparation of HeLa cell nuclear and cytosolic S100 extracts for in vitro splicing. Methods Mol. Biol., 118, 309-314.
46. Mayeda, A., Helfman, D.M. and Krainer, A.R. (1993) Modulation of exon skipping and inclusion by heterogeneous nuclear ribonucleoprotein A1 and pre-mRNA splicing factor SF2/ASF [published erratum appears in Mol. Cell. Biol. (1993) 13, 4458]. Mol. Cell. Biol., 13, 2993-3001.
47. Mayeda, A., Munroe, S.H., Caceres, J.F. and Krainer, A.R. (1994) Function of conserved domains of hnRNP A1 and other hnRNP A/B proteins. EMBO J., 13, 5483-5495.
48. Mayeda, A., Screaton, G.R., Chandler, S.D., Fu, X.D. and Krainer, A.R. (1999) Substrate specificities of SR proteins in constitutive splicing are determined by their RNA recognition motifs and composite pre-mRNA exonic elements. Mol. Cell. Biol., 19, 1853-1863.
49. Nelson, K.K. and Green, M.R. (1990) Mechanism for cryptic splice site activation during pre-mRNA splicing. Proc. Natl Acad. Sci. USA, 87, 6253-6257.
50. Reed, R. (1996) Initial splice-site recognition and pairing during pre-mRNA splicing. Curr. Opin. Genet. Dev., 6, 215-220.
51. Sawyer, S.T., Koury, M.J. and Bondurant, M.C. (1987) Large-scale procurement of erythropoietin-responsive erythroid cells: Assay for biological activity of erythropoietin. Methods Enzymol., 147, 340-352.
52. Schaal, T.D. and Maniatis, T. (1999) Multiple distinct splicing enhancers in the protein-coding sequences of a constitutively spliced pre-mRNA. Mol. Cell. Biol., 19, 261-273.
53. Schischmanoff, P.O., Winardi, R., Discher, D.E., Parra, M.K., Bicknese, S.E., Witkowska, H.E., Conboy, J.G. and Mohandas, N. (1995) Defining the minimal domain of protein 4.1 involved in spectrin-actin binding. J. Biol. Chem., 270, 21243-21250.
54. Si, Z.H., Rauch, D. and Stoltzfus, C.M. (1998) The exon splicing silencer in human immunodeficiency virus type 1 Tat exon 3 is bipartite and acts early in spliceosome assembly. Mol. Cell. Biol., 18, 5404-5413.
55. Siebel, C.W., Fresco, L.D. and Rio, D.C. (1992) The mechanism of somatic inhibition of Drosophila P-element pre-mRNA splicing: Multiprotein complexes at an exon pseudo-5′ splice site control U1 snRNP binding. Genes Dev., 6, 1386-1401.
56. Smith, C.W. and Valcarcel, J. (2000) Alternative pre-mRNA splicing: The logic of combinatorial control. Trends Biochem. Sci., 25, 381-388.
57. Staffa, A., Acheson, N.H. and Cochrane, A. (1997) Novel exonic elements that modulate splicing of the human fibronectin EDA exon. J. Biol. Chem., 272, 33394-33401.
58. Takakuwa, Y., Tchernia, G., Rossi, M., Benabadji, M. and Mohandas, N. (1986) Restoration of normal membrane stability to unstable protein 4.1-deficient membranes by incorporation of purified protein 4.1. J. Clin. Invest., 78, 80-85.
59. Tange, T.O., Damgaard, C.K., Guth, S., Valcarcel, J. and Kjems, J. (2001) The hnRNP A1 protein regulates HIV-1 tat splicing via a novel intron silencer element. EMBO J., 20, 5748-5758.
60. Wang, J. and Manley, J.L. (1997) Regulation of pre-mRNA splicing in metazoa. Curr. Opin. Genet. Dev., 7, 205-211.
61. Watakabe, A., Tanaka, K. and Shimura, Y. (1993) The role of exon sequences in splice site selection. Genes Dev., 7, 407-418.
62. Winardi, R., Discher, D., Kelley, C., Zon, L., Mays, K., Mohandas, N. and Conboy, J.G. (1995) Evolutionarily conserved alternative pre-mRNA splicing regulates structure and function of the spectrin-actin binding domain of erythroid protein 4.1. Blood, 86, 4315-4322.
63. Yang, X., Bani, M.R., Lu, S.J., Rowan, S., Ben-David, Y. and Chabot, B. (1994) The A1 and A1B proteins of heterogeneous nuclear ribonucleoparticles modulate 5′ splice site selection in vivo. Proc. Natl Acad. Sci. USA, 91, 6924-6928.
64. Yew, N.S., Choi, H.R., Gallarda, J.L. and Engel, J.D. (1987) Expression of cytoskeletal protein 4.1 during avian erythroid cellular maturation. Proc. Natl Acad. Sci. USA, 84, 1035-1039.
65. Zhu, J., Mayeda, A. and Krainer, A.R. (2001) Exon identity established through differential antagonism between exonic splicing silencer-bound hnRNP A1 and enhancer-bound SR proteins. Mol. Cell, 8, 1351-1361.