Mature erythrocyte membrane homeostasis is compromised by loss of the GATA1-FOG1 interaction

Blood

Volumn 119, Issue 11, 2012, Pages 2615-2623

  Hasegawa, Atsushi ^a   Shimizu, Ritsuko ^a   Mohandas, Narla ^b   Yamamoto, Masayuki ^a  

^a TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b NEW YORK BLOOD CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AQUAPORIN 1; ERYTHROCYTE BAND 3 PROTEIN; MEMBRANE PROTEIN; PROTEIN FOG1; REACTIVE OXYGEN METABOLITE; SPECTRIN; TRANSCRIPTION FACTOR GATA 1; UNCLASSIFIED DRUG;

ADULTHOOD; ALAS2 GENE; ANEMIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AQP1 GENE; ARTICLE; CANONICAL ANALYSIS; CELL MATURATION; CONTROLLED STUDY; DISEASE SEVERITY; ERYTHROCYTE MEMBRANE; GENE; GENE EXPRESSION; GENETIC CODE; HOMEOSTASIS; JAUNDICE; MOUSE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN FUNCTION; PROTEIN INTERACTION; SLC4A1 GENE; SPHEROCYTOSIS; SPNA1 GENE; SURVIVAL;

EID: 84858685700     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2011-09-382473     Document Type: Article

References (49)

1. Ohneda K, Yamamoto M. Roles of hematopoietic transcription factors GATA-1 and GATA-2 in the development of red blood cell lineage. Acta Haematol. 2002;108(4):237-245. (Pubitemid 35356700)
2. Shimizu R, Engel JD, Yamamoto M. GATA1-related leukaemias. Nat Rev Cancer. 2008;8(4):279-287. (Pubitemid 351430864)
3. Gutierrez L, Nikolic T, van Dijk TB, et al. Gata1 regulates dendritic-cell development and survival. Blood. 2007;110(6):1933-1941. (Pubitemid 47443907)
4. Fujiwara Y, Browne CP, Cunniff K,Goff SC, Orkin SH. Arrested development of embryonic red cell precursors in mouse embryos lacking transcription factor GATA-1. Proc Natl Acad Sci U S A. 1996;93(22):12355-12358. (Pubitemid 26367147)
5. Takahashi S, Onodera K, Motohashi H, et al. Arrest in primitive erythroid cell development caused by promoter-specific disruption of the GATA-1 gene. J Biol Chem. 1997;272(19):12611-12615. (Pubitemid 27203356)
6. Gutierrez L, Tsukamoto S, Suzuki M, et al. Ablation of Gata1 in adult mice results in aplastic crisis, revealing its essential role in steady-state and stress erythropoiesis. Blood. 2008;111(8):4375-7385.
7. Shimizu R, Takahashi S, Ohneda K, Engel JD, Yamamoto M. In vivo requirements for GATA-1 functional domains during primitive and definitive erythropoiesis. EMBO J. 2001;20(18):5250-5260. (Pubitemid 32910919)
8. Fox AH, Kowalski K, King GF, Mackay JP, Crossley M. Key residues characteristic of GATA N-fingers are recognized by FOG. J Biol Chem. 1998;273(50):33595-33603. (Pubitemid 29005746)
9. Trainor CD, Omichinski JG, Vandergon TL, Gronenborn AM, Clore GM, Felsenfeld G. A palindromic regulatory site within vertebrate GATA-1 promoters requires both zinc fingers of the GATA-1 DNA-binding domain for high-affinity interaction. Mol Cell Biol. 1996;16(5):2238-2247. (Pubitemid 26123744)
10. Tsang AP, Visvader JE, Turner CA, et al. FOG, a multitype zinc finger protein, acts as a cofactor for transcription factor GATA-1 in erythroid and megakaryocytic differentiation. Cell. 1997;90(1):109-119. (Pubitemid 28009423)
11. Crispino JD, Lodish MB, MacKay JP, Orkin SH. Use of altered specificity mutants to probe a specific protein-protein interaction in differentiation: the GATA-1:FOG complex. Mol Cell. 1999;3(2):219-228. (Pubitemid 29292622)
12. Kowalski K, Czolij R, King GF, Crossley M, Mackay JP. The solution structure of the N-terminal zinc finger of GATA-1 reveals a specific binding face for the transcriptional co-factor FOG. J Biomol NMR. 1999;13(3):249-262. (Pubitemid 29143532)
13. Ciovacco WA, Raskind WH, Kacena MA. Human phenotypes associated with GATA-1 mutations. Gene. 2008;427(1-2):1-6.
14. Nichols KE, Crispino JD, Poncz M, et al. Familial dyserythropoietic anaemia and thrombocytopenia due to an inherited mutation in GATA1. Nat Genet. 2000;24(3):266-270. (Pubitemid 30132195)
15. Chang AN, Cantor AB, Fujiwara Y, et al. GATA-factor dependence of the multitype zinc-finger protein FOG-1 for its essential role in megakaryopoiesis. Proc Natl Acad Sci U S A. 2002;99(14):9237-9242. (Pubitemid 34764597)
16. Shimizu R, Ohneda K, Engel JD, Trainor CD, Yamamoto M. Transgenic rescue of GATA-1-deficient mice with GATA-1 lacking a FOG-1 association site phenocopies patients with X-linked thrombocytopenia. Blood. 2004;103(7):2560- 2567. (Pubitemid 38393007)
17. Shimizu R, Kobayashi E, Engel JD, Yamamoto M. Induction of hyperproliferative fetal megakaryopoiesis by an N-terminally truncated GATA1 mutant. Genes Cells. 2009;14(9):1119-1131.
18. Liu J, Guo X, Mohandas N, Chasis JA, An X. Membrane remodeling during reticulocyte maturation. Blood. 2010;115(10):2021-2027.
19. Socolovsky M, Nam H, Fleming MD, Haase VH, Brugnara C, Lodish HF. Ineffective erythropoiesis in Stat5a(-/-)5b(-/-) mice due to decreased survival of early erythroblasts. Blood. 2001;98(12):3261-3273.
20. Kina T, Ikuta K, Takayama E, et al. The monoclonal antibody TER-119 recognizes a molecule associated with glycophorin A and specifically marks the late stages of murine erythroid lineage. Br J Haematol. 2000;109(2):280-287. (Pubitemid 30350706)
21. Auffray I, Marfatia S, de Jong K, et al. Glycophorin A dimerization and band 3 interaction during erythroid membrane biognesis: in vivo studies in human glycophorin A transgenic mice. Blood. 2001;97(9):2872-288.
22. Gallagher PG, Sabatino DE, Romana M, et al. A human beta-spectrin gene promoter directs high level expression in erythroid but not muscle or neural cells. J Biol Chem. 1999;274(10):6062-6073. (Pubitemid 29111010)
23. 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(3):1136-1143. (Pubitemid 30616885)
24. Boulanger L, Sabatino DE, Wong EY, et al. Erythroid expression of the human alpha-spectrin gene promoter is mediated by GATA-1- and NFE2-binding proteins. J Biol Chem. 2002;277(44):41563-41570. (Pubitemid 35257460)
25. Wong EY, Lin J, Forget BG, Bodine DM, Gallagher PG. Sequences downstream of the erythroid promoter are required for high level expression of the human alpha-spectrin gene. J Biol Chem. 2004;279(53):55024-55033. (Pubitemid 40066494)
26. Sahr KE, Daniels BP, Hanspal M. Identification of the proximal erythroid promoter region of the mouse anion exchanger gene. Blood. 1996;88(12):4500-4509. (Pubitemid 26419133)
27. Karacay B, Chang LS. Induction of erythrocyte protein 4.2 gene expression during differentiation of murine erythroleukemia cells. Genomics. 1999;59(1):6-17. (Pubitemid 29339867)
28. Steiner LA, Maksimova Y, Schulz V, et al. Chromatin architecture and transcription factor binding regulate expression of erythrocyte membrane protein genes. Mol Cell Biol. 2009;29(20):5399-5412.
29. Chen K, Liu J, Heck S, Chasis JA, An X, Mohandas N. Resolving the distinct stages in erythroid differentiation based on dynamic changes in membrane protein expression during erythropoiesis. Proc Natl Acad Sci U S A. 2009;106(41):17413-17418.
30. Delaunay J. The molecular basis of hereditary red cell membrane disorders. Blood Rev. 2007;21(1):1-20. (Pubitemid 46110925)
31. Williamson RC, Toye AM. Glycophorin A: Band 3 aid. Blood Cells Mol Dis. 2008;41(1):35-43.
32. Letting DL, Chen YY, Rakowski C, Reedy S, Blobel GA. Context-dependent regulation of GATA-1 by friend of GATA-1. Proc Natl Acad Sci U S A. 2004;101(2):476-481. (Pubitemid 38084661)
33. Pal S, Cantor AB, Johnson KD, et al. Coregulator-dependent facilitation of chromatin occupancy by GATA-1. Proc Natl Acad Sci U S A. 2004;101(4):980-985. (Pubitemid 38160570)
34. Jing H, Vakoc CR, Ying L, et al. Exchange of GATA factors mediates transitions in looped chromatin organization at a developmentally regulated gene locus. Mol Cell. 2008;29(2):232-242. (Pubitemid 351172817)
35. Johnson KD, Kim SI, Bresnick EH. Differential sensitivities of transcription factor target genes underlie cell type-specific gene expression profiles. Proc Natl Acad Sci U S A. 2006;103(43):15939-15944. (Pubitemid 44657571)
36. Perrotta S, Gallagher PG, Mohandas N. Hereditary Spherocytosis. Lancet. 2008;372(9647):1411-1426.
37. Peters LL, Swearingen RA, Andersen SG, et al. Identification of quantitative trait loci that modify the severity of hereditary spherocytosis in wan, a new mouse model of band-3 deficiency. Blood. 2004;103(8):3233-3240. (Pubitemid 38451705)
38. Southgate CD, Chishti AH, Mitchell B, Yi SJ, Palek J. Targeted disruption of the murine erythroid band 3 gene results in spherocytosis and severe haemolytic anaemia despite a normal membrane skeleton. Nat Genet. 1996;14(2):227-230. (Pubitemid 26338811)
39. Peters LL, Shivdasani RA, Liu SC, et al. Anion exchanger 1 (band 3) is required to prevent erythrocyte membrane surface loss but not to form the membrane skeleton. Cell. 1996;86(6):917-927. (Pubitemid 26336796)
40. Wandersee NJ, Birkenmeier CS, Bodine DM, Mohandas N, Barker JE. Mutations in the murine erythroid alpha-spectrin gene alter spectrin mRNA and protein levels and spectrin incorporation into the red blood cell membrane skeleton. Blood. 2003;101(1):325-330. (Pubitemid 36025926)
41. Nakano M, Ohneda K, Yamamoto-Mukai H, et al. Transgenic over-expression of GATA-1 mutant lacking N-finger domain causes hemolytic syndrome in mouse erythroid cells. Genes Cells. 2005;10(1):47-62. (Pubitemid 40352617)
42. Ma T, Yang B, Gillespie A, Carlson EJ, Epstein CJ, Verkman AS. Severely impaired urinary concentrating ability in transgenic mice lacking aquaporin-1 water channels. J Biol Chem. 1998;273(8):4296-4299. (Pubitemid 28103161)
43. Mathai JC, Mori S, Smith BL, et al. Functional analysis of aquaporin-1 deficient red cells. The Colton-null phenotype. J Biol Chem. 1996;271(3):1309-1313.
44. Blanc L, Liu J, Vidal M, Chasis JA, An X, Mohandas N. The water channel aquaporin-1 partitions into exosomes during reticulocyte maturation: implication for the regulation of cell volume. Blood. 2009;114(18):3928-3934.
45. Wang S, Dale G, Song P, Viollet B, Xou M. AMPKa1 deletion shortens erythrocyte life span in mice. J Biol Chem. 2010;285(26):19976-19985.
46. An X, Mohandas N. Disorders of red cell membrane. Br J Haematol. 2008;141(3):367-375. (Pubitemid 351521152)
47. Gallagher PG, Nilson DG, Wong C, et al. A dinucleotide deletion in the ankyrin promoter alters gene expression, transcription initiation and TFIID complex formation in hereditary spherocytosis. Hum Mol Genet. 2005;14(17):2501-2509. (Pubitemid 41236063)
48. Siatecka M, Sahr KE, Andersen SG, et al. Severe anemia in the Nan mutant mouse caused by sequence-selective disruption of erythroid Krüppellike factor. Proc Natl Acad Sci U S A. 2010;107(34):15151-15156.
49. Nilson DG, Sabatino DE, Bodine DM, Gallagher PG. Major erythrocyte membrane protein genes in EKLF-deficient mice. Exp Hematol. 2006;34(6):705-712. (Pubitemid 43737096)