Alternative 5′ exons and differential splicing regulate expression of protein 4.1R isoforms with distinct N-termini

Blood

Volumn 101, Issue 10, 2003, Pages 4164-4171

  Parra, Marilyn K ^b   Gee, Sherry L ^b   Koury, Mark J ^b   Mohandas, Narla ^b   Conboy, John G ^a  

^a LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

ERYTHROCYTE BAND 4.1 PROTEIN; ISOPROTEIN; PROTEIN 4 1 R; UNCLASSIFIED DRUG; CYTOSKELETON PROTEIN; MEMBRANE PROTEIN; NEURONAL MEMBRANE CYTOSKELETAL PROTEIN 4.1; NEUROPEPTIDE; PRIMER DNA; PROTEIN;

ALTERNATIVE RNA SPLICING; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; DNA FLANKING REGION; ERYTHROBLAST; ERYTHROID CELL; EXON; GENE EXPRESSION REGULATION; GENE MUTATION; GENE SEQUENCE; GENETIC CODE; GENETIC TRANSCRIPTION; GENOME; GENOMICS; HUMAN; HUMAN GENOME; HUMAN TISSUE; MOUSE; NONHUMAN; NORTHERN BLOTTING; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN SYNTHESIS; SEQUENCE ANALYSIS; TRANSCRIPTION INITIATION SITE; TRANSLATION INITIATION; ANIMAL; CONSENSUS SEQUENCE; GENE AMPLIFICATION; GENETICS; METABOLISM; MOLECULAR GENETICS; POLYMERASE CHAIN REACTION; SEQUENCE ALIGNMENT;

ALTERNATIVE SPLICING; ANIMALS; BASE SEQUENCE; BLOTTING, NORTHERN; CONSENSUS SEQUENCE; CYTOSKELETAL PROTEINS; DNA PRIMERS; ERYTHROBLASTS; EXONS; GENE AMPLIFICATION; HUMANS; MEMBRANE PROTEINS; MICE; MOLECULAR SEQUENCE DATA; NEUROPEPTIDES; POLYMERASE CHAIN REACTION; PROMOTER REGIONS (GENETICS); PROTEIN ISOFORMS; PROTEINS; SEQUENCE ALIGNMENT; TRANSCRIPTION, GENETIC;

EID: 0038264415     PISSN: 00064971     EISSN: None     Source Type: Journal    
DOI: 10.1182/blood-2002-06-1796     Document Type: Article

References (58)

1. Tchernia G, Mohandas N, Shohet SB. Deficiency of skeletal membrane protein band 4.1 in homozygous hereditary elliptocytosis: implications for erythrocyte membrane stability. J Clin Invest. 1981;68:454-460.
2. Takakuwa Y, Tchernia G, Rossi M, Benabadji M, Mohandas N. Restoration of normal membrane stability to unstable protein 4.1-deficient membranes by incorporation of purified protein 4.1. J Clin Invest. 1986;78:80-85.
3. Shi ZT, Afzal V, Coller B, et al. Protein 4.1R-deficient mice are viable but have erythroid membrane skeleton abnormalities. J Clin Invest. 1999;103:331-340.
4. Han BG, Nunomura W, Takakuwa Y, Mohandas N, Jap BK. Protein 4.1R core domain structure and insights into regulation of cytoskeletal organization. Nat Struct Biol. 2000;7:871-875.
5. Correas I. Characterization of isoforms of protein 4.1 present in the nucleus. Biochem J. 1991;279:581-585.
6. De Carcer G, Lallena MJ, Correas I. Protein 4.1 is a component of the nuclear matrix of mammalian cells. Biochem J. 1995;312:871-877.
7. Krauss SW, Larabell CA, Lockett S, et al. Structural protein 4.1 in the nucleus of human cells: dynamic rearrangements during cell division. J Cell Biol. 1997;137:275-289.
8. Lallena MJ, Correas I. Transcription-dependent redistribution of nuclear protein 4.1 to SC35-enriched nuclear domains. J Cell Sci. 1997;110:239-247.
9. Krauss SW, Chasis JA, Rogers C, Mohandas N, Krockmalnic G, Penman S. Structural protein 4.1 is located in mammalian centrosomes. Proc Natl Acad Sci U S A. 1997;94:7297-7302.
10. Maltagajasingh SN, Huang SC, Hartenstein JS, Benz EJ Jr. Characterization of the interaction between protein 4.1R and ZO-2: a possible link between the tight junction and the actin cytoskeleton. J Biol Chem. 2000;275:30573-30585.
11. Kontrogianni-Konstantopoulos A, Huang SC, Benz EJ Jr. A nonerythroid isoform of protein 4.1R interacts with components of the contractile apparatus in skeletal myofibers. Mol Biol Cell. 2000;11:3805-3817.
12. Walensky LD, Shi ZT, Blackshaw S, et al. Neurobehavioral deficits in mice lacking the erythrocyte membrane cytoskeletal protein 4.1. Curr Biol. 1998;8:1269-1272.
13. Nunomura W, Takakuwa Y, Tokimitsu R, Krauss SW, Kawashima M, Mohandas N. Regulation of CD44-protein 4.1 interaction by Ca2+ and calmodulin: implications for modulation of CD44-ankyrin interaction. J Biol Chem. 1997;272:30322-30328.
14. Hemming NJ, Anstee DJ, Staricoff MA, Tanner MJ, Mohandas N. Identification of the membrane attachment sites for protein 4.1 in the human erythrocyte. J Biol Chem. 1995;270:5360-5366.
15. Marfatia SM, Leu RA, Branton D, Chishti AH. Identification of the protein 4.1 binding interface on glycophorin C and p55, a homologue of the Drosophila discs-large tumor suppressor protein. J Biol Chem. 1995;270:715-719.
16. Cohen AR, Wood DF, Marfatia SM, Walther Z, Chishti AH, Anderson JM. Human CASK/LIN-2 binds syndecan-2 and protein 4.1 and localizes to the basolateral membrane of epithelial cells. J Cell Biol. 1998;142:129-138.
17. Lue RA, Marfatia SM, Branton D, Chishti AH. Cloning and characterization of hdlg: the human homologue of the Drosophila discs large tumor suppressor binds to protein 4.1. Proc Natl Acad Sci U S A. 1994;91:9818-9822.
18. Hou CL, Tang C, Roffler SR, Tang TK. Protein 4.1R binding to elF3-p44 suggests an interaction between the cytoskeletal network and the translation apparatus. Blood. 2000;96:747-753.
19. Hung LY, Tang CJ, Tang TK. Protein 4.1 R-135 interacts with a novel centrosomal protein (CPAP) which is associated with the gamma-tubulin complex. Mol Cell Biol. 2000;20:7813-7825.
20. Lallena MJ, Martinez C, Valcarcel J, Correas I. Functional association of nuclear protein 4.1 with pre-mRNA splicing factors. J Cell Sci. 1998;111:1963-1971.
21. Tang CJ, Tang TK. The 30-kD domain of protein 4.1 mediates its binding to the carboxyl terminus of plCln, a protein involved in cellular volume regulation. Blood. 1998;92:1442-1447.
22. Huang JP, Tang CJ, Kou GH, Marchesi VT, Benz EJ Jr, Tang TK. Genomic structure of the locus encoding protein 4.1: structural basis for complex combinational patterns of tissue-specific alternative RNA splicing. J Biol Chem. 1993;268:3758-3766.
23. Baklouti F, Huang SC, Vulliamy TJ, Delaunay J, Benz EJ Jr. Organization of the human protein 4.1 genomic locus: new insights into the tissue-specific alternative splicing of the pre-mRNA. Genomics. 1997;39:289-302.
24. Conboy J. The role of alternative pre-mRNA splicing in regulating the structure and function of skeletal protein 4.1. Proc Soc Exp Biol Med. 1999;220:73-78.
25. Gascard P, Lee G, Coulombel L, et al. Characterization of multiple isoforms of protein 4.1R expressed during erythroid terminal differentiation. Blood. 1998;92:4404-4414.
26. Chasis JA, Coulombel L, Conboy J, et al. Differentiation-associated switches in protein 4.1 expression: synthesis of multiple structural isoforms during normal human erythropoiesis. J Clin Invest. 1993;91:329-338.
27. Baklouti F, Huang SC, Tang TK, Delaunay J, Marchesi VT, Benz EJ Jr. Asynchronous regulation of splicing events within protein 4.1 pre-mRNA during erythroid differentiation. Blood. 1996;87:3934-3941.
28. Gee SL, Aoyagi K, Lersch R, Hou V, Wu M, Conboy JG. Alternative splicing of protein 4.1R exon 16: ordered excision of flanking introns ensures proper splice site choice. Blood. 2000;95:692-699.
29. Horton RM, Hunt HD, Ho SN, Pullen JK, Pease LR. Engineering hybrid genes without the use of restriction enzymes: gene splicing by overlap extension. Gene. 1989;77:61-68.
30. Sawyer ST, Koury MJ, Bondurant MC. Large-scale procurement of erythropoietin-responsive erythroid cells: assay for biological activity of erythropoietin. Methods Enzymol. 1987;147:340-352.
31. Koury MJ, Sawyer ST, Bondurant MC. Splenic erythroblasts in anemia-inducing Friend disease: a source of cells for studies of erythropoietin-mediated differentiation. J Cell Physiol. 1984;121:526-532.
32. Scherf M, Klingenhoff A, Werner T. Highly specific localization of promoter regions in large genomic sequences by PromoterInspector: a novel context analysis approach. J Mol Biol. 2000;297:599-606.
33. Koury MJ, Bondurant MC, Mueller TJ. The role of erythropoietin in the production of principal erythrocyte proteins other than hemoglobin during terminal erythroid differentiation. J Cell Physiol. 1986;126:259-265.
34. Hou VC, Lersch R, Gee SL, et al. Decrease in hnRNP A/B expression during erythropoiesis mediates a pre-mRNA splicing switch. EMBO J. 2002;21:6195-6204.
35. Hanspal M, Hanspal JS, Kalraiya R, et al. Asynchronous synthesis of membrane skeletal proteins during terminal maturation of murine erythroblasts. Blood. 1992;80:530-539.
36. Conboy JG, Chan JY, Chasis JA, Kan YW, Mohandas N. Tissue- and development-specific alternative RNA splicing regulates expression of multiple isoforms of erythroid membrane protein 4.1. J Biol Chem. 1991;266:8273-8280.
37. Schischmanoff PO, Yaswen P, Parra MK, et al. Cell shape-dependent regulation of protein 4.1 alternative pre-mRNA splicing in mammary epithelial cells. J Biol Chem. 1997;272:10254-10259.
38. Mattagajasingh SN, Huang SC, Hartenstein JS, Snyder M, Marchesi VT, Benz EJ. A nonerythroid isoform of protein 4.1R interacts with the nuclear mitotic apparatus (NuMA) protein. J Cell Biol. 1999;145:29-43.
39. Anderson RA, Correas I, Mazzucco C, Castle JD, Marchesi VT. Tissue-specific analogues of erythrocyte protein 4.1 retain functional domains. J Cell Biochem. 1988;37:269-284.
40. Bishop TR, Miller MW, Beall J, Zon LI, Dierks P. Genetic regulation of delta-aminolevulinate dehydratase during erythropoiesis. Nucleic Acids Res. 1996;24:2511-2518.
41. Kaya AH, Plewinska M, Wong DM, Desnick RJ, Wetmur JG. Human delta-aminolevulinate dehydratase (ALAD) gene: structure and alternative splicing of the erythroid and housekeeping mRNAs. Genomics. 1994;19:242-248.
42. Grandchamp B, De VH, Beaumont C, Chretien S, Walter O, Nordmann Y. Tissue-specific expression of porphobilinogen deaminase: two isoenzymes from a single gene. Eur J Biochem. 1987;162:105-110.
43. Romeo PH, Mignotte V, Raich N, et al. Regulated expression of the erythroid-specific-promoter of the human PBG-D gene during erythroid differentiation. Prog Clin Biol Res. 1989:359-366.
44. Aizencarig GI, Bishop DF, Forrest D, Astrin KH, Desnick RJ. Uroporphyrinogen III synthase: an alternative promoter controls erythroid-specific expression in the murine gene. J Biol Chem. 2000;275:2295-2304.
45. Sahr KE, Daniels BP, Hanspal M. Identification of the proximal erythroid promoter region of the mouse anion exchanger gene. Blood. 1996;88:4500-4509.
46. Gallagher PG, Romana M, Tse WT, Lux SE, Forget BG. The human ankyrin-1 gene is selectively transcribed in erythroid cell lines despite the presence of a housekeeping-like promoter. Blood. 2000;96:1136-1143.
47. Birkenmeier CS, Sharp JJ, Gifford EJ, Deveau SA, Barker JE. An alternative first exon in the distal end of the erythroid ankyrin gene leads to production of a small isoform containing an NH2-terminal membrane anchor. Genomics. 1998;50:79-88.
48. Chin K, Yu X, Beleslin-Cokic B, Liu C, Shen K, Mohrenweiser HW, Noguchi CT. Production and processing of erythropoietin receptor transcripts in brain. Brain Res Mol Brain Res. 2000;81:29-42.
49. Moroni E, Cairns L, Ottolenghi S, et al. Expression in hematopoietic cells of GATA-1 transcripts from the alternative "testis" promoter during development and cell differentiation. Biochem Biophys Res Commun. 1997;231:299-304.
50. Vannucchi AM, Linari S, Lin CS, Koury MJ, Bondurant MC, Migliaccio AR. Increased expression of the distal, but not of the proximal, Gata1 transcripts during differentiation of primary erythroid cells. J Cell Physiol. 1999;180:390-401.
51. Toki T, Arai K, Terui K, et al. Functional characterization of the two alternative promoters of human p45 NF-E2 gene. Exp Hematol. 2000;28:1113-1119.
52. Bentley D. Coupling RNA polymerase II transcription with pre-mRNA processing. Curr Opin Cell Biol. 1999;11:347-351.
53. Hirose Y, Manley JL. RNA polymerase II and the integration of nuclear events. Genes Dev. 2000;14:1415-1429.
54. Proudfoot N. Connecting transcription to messenger RNA processing. Trends Biochem Sci. 2000;25:290-293.
55. Maniatis T, Reed R. An extensive network of coupling among gene expression machines. Nature. 2002;416:499-506.
56. Cramer P, Pesce CG, Baralle FE, Kornblihtt AR. Functional association between promoter structure and transcript alternative splicing. Proc Natl Acad Sci U S A. 1997;94:11456-11460.
57. Cramer P, Caceres JF, Cazalla D, et al. Coupling of transcription with alternative splicing: RNA pol II promoters modulate SF2/ASF and 9G8 effects on an exonic splicing enhancer. Mol Cell. 1999;4:251-258.
58. Luque CM, Lallena MJ, Perez-Ferreiro CM, et al. The N-terminal 209-aa domain of high molecular-weight 4.1R isoforms abrogates 4.1R targeting to the nucleus. Proc Natl Acad Sci U S A. 1999;96:14925-14930.