Repression via the GATA box is essential for tissue-specific erythropoietin gene expression

Blood

Volumn 111, Issue 10, 2008, Pages 5223-5232

  Obara, Naoshi ^a,b   Suzuki, Norio ^a   Kim, Kibom ^a   Nagasawa, Toshiro ^b   Imagawa, Shigehiko ^b   Yamamoto, Masayuki ^a,c  

^a UNIVERSITY OF TSUKUBA   (Japan)

^b Graduate School of Comprehensive Human Sciences   (Japan)

^c TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ERYTHROPOIETIN; GREEN FLUORESCENT PROTEIN; TRANSCRIPTION FACTOR GATA; TRANSCRIPTION FACTOR GATA 2; TRANSCRIPTION FACTOR GATA 3;

ANEMIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL HYPOXIA; CELL POPULATION; CELL STRUCTURE; CONTROLLED STUDY; EPITHELIUM CELL; GENE EXPRESSION; GENE LOCUS; GENE MUTATION; GENE REPRESSION; IMMUNOHISTOCHEMISTRY; KIDNEY CELL; LEYDIG CELL; LIVER CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN MOTIF; REGULATORY MECHANISM; SINGLE NUCLEOTIDE POLYMORPHISM; TRANSGENIC MOUSE; ANIMAL; ANOXIA; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; KIDNEY; LIVER; METABOLISM; NERVE CELL; PHYSIOLOGY; TISSUE DISTRIBUTION;

AMINO ACID MOTIFS; ANEMIA; ANIMALS; ANOXIA; ERYTHROPOIETIN; GATA2 TRANSCRIPTION FACTOR; GATA3 TRANSCRIPTION FACTOR; GENE EXPRESSION REGULATION; KIDNEY; LIVER; MICE; MICE, TRANSGENIC; NEURONS; PROMOTER REGIONS (GENETICS); TISSUE DISTRIBUTION;

EID: 46749127450     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2007-10-115857     Document Type: Article

References (48)

1. Ebert BL, Bunn HF. Regulation of the erythropoietin gene. Blood. 1999;94:1864-1877.
2. 125I-erythropoietin by the placenta. J Clin Invest. 1988;82:154-159.
3. Tarumoto T, Imagawa S, Ohmine K, et al. N(G)-monomethyl-L-arginine inhibits erythropoietin gene expression by stimulating GATA-2. Blood. 2000;96:1716-1722.
4. Obara N, Imagawa S, Nakano Y, Suzuki N, Yamamoto M, Nagasawa T. Suppression of erythropoietin gene expression by cadmium depends on inhibition of HIF-1, not stimulation of GATA-2. Arch Toxicol. 2003;77:267-273.
5. Jelkmann W. Erythropoietin. J Endocrinol Invest. 2003;26:832-837.
6. Goldberg MA, Glass GA, Cunningham JM, Bunn HF. The regulated expression of erythropoietin by two human hepatoma cell lines. Proc Natl Acad Sci U S A. 1987;84:7972-7976.
7. Semenza GL, Wang GL. Anuclear factor induced by hypoxia via de novo protein synthesis binds to human erythropoietin gene enhancer at a site required for transcriptional activation. Mol Cell Biol. 1992;12:5447-5454.
8. Makita T, Hernandez HG, Chen TH, Wu H, Rothenberg EV, Sucov HM. A developmental transition in definitive erythropoiesis: erythropoietin expression is sequentially regulated by retinoic acid receptors and HNF4. Genes Dev. 2001;15:889-901.
9. Koury MJ. Erythropoietin: the story of hypoxia and a finely regulated hematopoietic hormone. Exp Hematol. 2005;33:1263-1270.
10. Imagawa S, Yamamoto M, Miura Y. Negative regulation of the erythropoietin gene expression by the GATA transcription factors. Blood. 1997;89:1430-1439.
11. Imagawa S, Suzuki N, Ohmine K, et al. GATA suppresses erythropoietin gene expression through GATA site in mouse erythropoietin gene promoter. Int J Hematol. 2002;75:376-381.
12. Semanza GL, Dureza RC, Traystman MD, Gear-hart JD, Antonarakis SE. Human erythropoietin gene expression in transgenic mice: multiple transcription initiation site and cis-acting regulatory elements. Mol Cell Biol. 1990;10:930-938.
13. Semenza GL, Koury ST, Nejfelt MK, Gearhart JD, Antonarakis SE. Cell-type-specific and hypoxia: inducible expression of the human erythropoietin gene in transgenic mice. Proc Natl Acad Sci U S A. 1991;88:8725-8729.
14. Loya F, Yang Y, Lin H, Goldwasser E, Albitar M. Transgenic mice carrying the erythropoietin gene promoter linked to lacZ express the reporter in proximal convoluted tubule cells after hypoxia. Blood. 1994;84:1831-1836.
15. Madan A, Lin C, Hatch SL II, Curtin PT. Regulated basal, inducible, and tissue-specific human erythropoietin gene expression in transgenic mice requires multiple cis DNA sequences. Blood. 1995;85:2735-2741.
16. Maxwell AP, Lappin TR, Johnston CF, Bridges JM, McGeown MG. Erythropoietin production in kidney tubular cells. Br J Haematol. 1990;74:535-539.
17. Burlington H, Cronkite EP, Reincke U, Zanjani ED. Erythropoietin production in cultures of goat renal glomeruli. Proc Natl Acad Sci U S A. 1972;69:3547-3550.
18. Kurtz A, Jelkmann W, Sinowaitz F, Bauer C. Renal mesangial cell cultures as a model for study of erythropoietin production. Proc Natl Acad Sci U S A. 1983;80:4008-4011.
19. Koury ST, Bondurant MC, Koury MJ. Localization of erythropoietin synthesizing cells in murine kidneys by in situ hybridization. Blood. 1988;71:524-527.
20. Lacombe C, Da Silva JL, Bruneval P, et al. Peritubular cells are the site of erythropoietin synthesis in the murine hypoxic kidney. J Clin Invest. 1988;81:620-623.
21. Schuster SJ, Wilson JH, Erselv AJ, Caro J. Cellular sites of extrarenal and renal erythropoietin production in anaemic rats. Br J Haematol. 1992;81:153-159.
22. Bachmann S, Le HM, Eckardt KU. Co-localization of erythropoietin mRNA and ecto-5′-nucleotidase immunoreactivity in peritubular cells of rat renal cortex indicates that fibroblasts produce erythropoietin. J Histochem Cytochem. 1993;41:335-341.
23. Maxwell PH, Osmond MK, Pugh CW, et al. Identification of the renal erythropoietin-producing cells using transgenic mice. Kidney Int. 1993;44:1149-1162.
24. Suzuki N, Obara N, Yamamoto M. Use of gene manipulated mice in the study of erythropoietin gene expression. Methods Enzymol. 2007;435:157-177.
25. Yu D, Ellis HM, Lee EC, Jenkins NA, Copeland NG, Court DL. An efficient recombination system for chromosome engineering in Escherichia coli. Proc Natl Acad Sci U S A. 2000;97:5978-5983.
26. Lee EC, Yu D, Martinez J, et al. A highly efficient Escherichia coli-based chromosome engineering system adapted for recombinogenic targeting and subcloning of BAC DNA. Genomics. 2001;73:56-65.
27. Ito W, Ishiguro H, Kurosawa Y. A general method for introducing a series of mutations into cloned DNA using the polymerase chain reaction. Gene. 1991;102:67-70.
28. Chrast R, Scott HS, Antonarakis SE. Linearization and purification of BAC DNA for the development of transgenic mice. Transgenic Res. 1999;8:147-150.
29. Suzuki N, Suwabe N, Ohneda O, et al. Identification and characterization of 2 types of erythroid progenitors that express GATA-1 at distinct levels. Blood. 2003;102:3575-3583.
30. Suzuki N, Ohneda O, Minegishi N, et al. Combinatorial Gata2 and Sca1 expression defines hematopoietic stem cells in the bone marrow niche. Proc Natl Acad Sci U S A. 2006;103:2202-2207.
31. Hendriks RW, Nawjin MC, Engel JD, van Doorninck H, Grosveld F, Karis A. Expression of the transcription factor GATA-3 is required for the development of the earliest T cell progenitors and correlates with stages of cellular proliferation in the thymus. Eur J Immunol. 1999;29:1912-1918.
32. The Standards for Human Care and Use of Laboratory Animals of the University of Tsukuba. Tsukuba, Japan; 2005.
33. Kobayashi T, Yanase H, Iwanaga T, Sasaki R, Nagao M. Epididymis is a novel site of erythropoietin production in mouse reproductive organs. Biochem Biophys Res Commun. 2002;296:145-151.
34. Ohneda K, Shimizu R, Nishimura S, et al. A mini gene containing four discrete cis elements recapitulates GATA-1 gene expression in vivo. Genes Cells. 2002;7:1243-1254.
35. Koury ST, Koury MJ, Bondurant MC, Caro J, Graber SE. Quantitation of erythropoietin-producing cells in kidneys of mice by in situ hybridization: correlation with hematocrit, renal erythropoietin mRNA, and serum erythropoietin concentration. Blood. 1989;74:645-651.
36. Aird WC, Parvin JD, Sharp PA, Rosenberg RD. The interaction of GATA-binding proteins and basal transcription factors with GATA box-containing core promoters: a model of tissue-specific gene expression. J Biol Chem. 1994;269:883-889.
37. Uchida S, Matsumura Y, Rai T, Sasaki S, Marumo F. Regulation of aquaporin-2 gene transcription by GATA-3. Biochem Biophys Res Commun. 1997;232:65-68.
38. Bruno MD, Korfhagen TR, Liu C, Morrisey EE, Whitsett JA. GATA-6 activates transcription of surfactant protein A. J Biol Chem. 2000;275:1043-1049.
39. Keijzer R, van Tuyl M, Meijers C, et al. The transcription factor GATA6 is essential for branching morphogenesis and epithelial cell differentiation during fetal pulmonary development. Development. 2001;128:503-511.
40. Liu C, Glasser SW, Wan H, Whitsett JA. GATA-6 and thyroid transcription factor-1 directly interact and regulate surfanctant protein-C gene expression. J Biol Chem. 2002;277:4519-4525.
41. Brines M, Cerami A. Discovering erythropoietin's extra-hematopoietic functions: biology and clinical promise. Kidney Int. 2006;70:246-250.
42. Suzuki N, Ohneda O, Takahashi S, et al. Erythroid-specific expression of the erythropoietin receptor rescued its null mutant mice from lethality. Blood. 2002;100:2279-2288.
43. Yamamoto M, Ko LJ, Leonard MW, Beug H, Orkin SH, Engel JD. Activity and tissue-specific expression of the transcription factor NF-E1 multigene family. Genes Dev. 1990;4:1650-1662.
44. Tong Q, Dalgin G, Xu H, Ting CN, Leiden JM, Hotamisligil GS. Function of GATA transcription factors in preadipocyte-adipocyte transision. Science. 2000;290:134-138.
45. Shoemaker CB, Mitsock LD. Murine erythropoietin gene: cloning, expression, and human gene homology. Mol Cell Biol. 1986;6:849-858.
46. Kuhn EJ, Geyer PK. Genomic insulators: connecting properties to mechanism. Curr Opin Cell Biol. 2003;15:259-265.
47. Thorling EB. Paraneoplastic erythrocytosis and inappropriate erythropoietin production: a review. Scand J Haematol. 1972;17:1-166.
48. Sakamoto S, Igarashi T, Osumi N, et al. Erythropoietin-producing renal cell carcinoma in chronic hemodialysis patients: a report of two cases. Int J Urol. 2003;10:49-51.