The mouse gene for hypoxia-inducible factor-1α. Genomic organization, expression and characterization of an alternative first exon and 5' flanking sequence

European Journal of Biochemistry

Volumn 246, Issue 1, 1997, Pages 155-165

  Wenger, Roland H ^a   Rolfs, Andreas ^a   Kvietikova, Ivica ^a   Spielmann, Patrick ^a   Zimmermann, Dieter R ^a   Gassmann, Max ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Erythropoietin; Gene expression; Hypoxia; Promoter; Transcription

Indexed keywords

CARRIER PROTEIN; HYPOXIA INDUCIBLE FACTOR 1; MESSENGER RNA; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL LINE; CONTROLLED STUDY; GENETIC ANALYSIS; HYPOXIA; MOLECULAR CLONING; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ANALYSIS; PROTEIN FAMILY; PROTEIN STRUCTURE; RNA ANALYSIS; TRANSCRIPTION INITIATION;

EID: 0030916245     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1432-1033.1997.t01-1-00155.x     Document Type: Article

References (69)

1. Jelkmann, W. (1992) Erythropoietin: structure, control of production, and function, Physiol. Rev. 72, 449-489.
2. Fandrey, J. (1995) Hypoxia-inducible gene expression, Resp. Physiol. 101, 1-10.
3. Wang, G. L. & Semenza, G. L. (1996) Oxygen sensing and response to hypoxia by mammalian cells, Redox Report 2, 89-96.
4. Bunn, H. F. & Poyton, R. O. (1996) Oxygen sensing and molecular adaptation to hypoxia, Physiol. Rev. 76, 839-885.
5. Shweiki, D., Itin, A., Soffer, D. & Keshet, E. (1992) Vascular endothelial growth factor induced by hypoxia may mediate hypoxia-initiated angiogenesis, Nature 359, 843-845.
6. Stein, I., Neeman, M., Shweiki, D., Itin, A. & Keshet, E. (1995) Stabilization of vascular endothelial growth factor mRNA by hypoxia and hypoglycemia and coregulation with other ischemia-induced genes, Mol. Cell. Biol. 15, 5363-5368.
7. Ebert, B. L., Firth, J. D. & Ratcliffe, P. J. (1995) Hypoxia and mitochondrial inhibitors regulate expression of glucose transporter-1 via distinct cis-acting sequences, J. Biol. Chem. 270, 29083-29089.
8. Ebert, B. L., Gleadle, J. M., O'Rourke, J. F., Bartlett, S. M., Poulton, J. & Ratcliffe, P. J. (1996) Isoenzyme-specific regulation of genes involved in energy metabolism by hypoxia: similarities with the regulation of erythropoietin, Biochem. J. 313, 809-814.
9. Semenza, G. L., Roth, P. H., Fang, H.-M. & Wang, G. L. (1994) Transcriptional regulation of genes encoding glycolytic enzymes by hypoxia-inducible factor 1, J. Biol. Chem. 269, 23757-23763.
10. Firth, J. D., Ebert, B. L., Pugh, C. W. & Ratcliffe, P. J. (1994) Oxygen-regulated control elements in the phosphoglycerate kinase 1 and lactate dehydrogenase A genes: similarities with the erythropoietin 3′ enhancer, Proc. Natl Acad. Sci. USA 91, 6496-6500.
11. Firth, J. D., Ebert, B. L. & Ratcliffe, P. J. (1995) Hypoxic regulation of lactate dehydrogenase A. Interaction between hypoxia-inducible factor 1 and cAMP response elements, J. Biol. Chem. 270, 21021-21027.
12. Semenza, G. L., Jiang, B.-H., Leung, S. W., Passantino, R., Concordet, J.-P., Maire, P. & Giallongo, A. (1996) Hypoxia response elements in the aldolase A, enolase 1, and lactate dehydrogenase A gene promoters contain essential binding sites for hypoxia-inducible factor 1, J. Biol. Chem. 271, 32529-32537.
13. Semenza, G. L. (1996) Transcriptional regulation by hypoxia-inducible factor 1. Molecular mechanisms of oxygen homeostasis, Trends Cardiovasc. Med. 6, 151-157.
14. Semenza, G. L. & Wang, G. L. (1992) A nuclear factor induced by hypoxia via de novo protein synthesis binds to the human erythropoietin gene enhancer at a site required for transcriptional activation, Mol. Cell. Biol. 12, 5447-5454.
15. Levy, A. P., Levy, N. S., Wegner, S. & Goldberg, M. A. (1995) Transcriptional regulation of the rat vascular endothelial growth factor gene by hypoxia, J. Biol. Chem. 270, 13333-13340.
16. Liu, Y., Cox, S. R., Morita, T. & Kourembanas, S. (1995) Hypoxia regulates vascular endothelial growth factor gene expression in endothelial cells, Circ. Res. 77, 638-643.
17. Norris, M. L. & Millhorn, D. E. (1995) Hypoxia-induced protein binding to unresponsive sequences on the tyrosine hydroxylase gene, J. Biol. Chem. 270, 23774-23779.
18. Forsythe, J. A., Jiang, B.-H., Iyer, N. V., Agani, F., Leung, S. W., Koos, R. D. & Semenza, G. L. (1996) Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1, Mol. Cell. Biol. 16, 4604-4613.
19. Li, H., Ko, H. P. & Whitlock J. P. Jr (1996) Induction of phosphoglycerate kinase 1 gene expression by hypoxia. Roles of ARNT and HIF1α, J. Biol. Chem. 271, 21262-21267.
20. Melillo, G. Musso, T., Sica, A., Taylor, L. S., Cox, G. W. & Varesio, L. (1995) A hypoxia-responsive element mediates a novel pathway of activation of the inducible nitric oxide synthase promoter, J. Exp. Med. 182, 1683-1693.
21. Estes, S. D., Stoler, D. L. & Anderson, G. R. (1995) Anoxic induction of a sarcoma virus-related VL30 retrotransposon is mediated by a cis-acting element which binds hypoxia-inducible factor 1 and an anoxia-inducible factor, J. Virol. 69, 6335-6341.
22. Maxwell, P. H., Pugh, C. W. & Ratcliffe, P. J. (1993) Inducible operation of the erythropoietin 3′ enhancer in multiple cell lines: Evidence for a widespread oxygen-sensing mechanism, Proc. Natl Acad. Sci. USA 90, 2423-2427.
23. Wang, G. L. & Semenza, G. L. (1993) General involvement of hypoxia-induciblc factor 1 in transcriptional response to hypoxia, Proc. Natl Acad. Sci. USA 90, 4304-4308.
24. Nagao, M., Ebert, B. L., Ratcliffe, P. J. & Pugh, C. W. (1996) Drosophila melanogaster SL2 cells contain a hypoxically inducible DNA binding complex which recognises mammalian HIF-1 binding sites, FEBS Lett. 387, 161-166.
25. Wang, G. L. & Semenza, G. L. (1995) Purification and characterization of hypoxia-inducible factor 1, J. Biol. Chem. 270, 1230-1237.
26. 2 tension, Proc. Natl Acad. Sci. USA 92, 5510-5514.
27. Poellinger, L. (1995) Mechanisms of signal transduction by the basic helix-loop-helix dioxin receptor, in Inducible gene expression (Baeuerle, P. A., ed.) vol. 1, pp. 177-205, Birkhäuser Verlag, Basel.
28. Hankinson, O. (1995) The aryl hydrocarbon receptor complex, Annu. Rev. Pharmacol. Toxicol. 35, 307-340.
29. Isaac, D. D. & Andrew, D. J. (1996) Tubulogenesis in Drosophila: a requirement for the trachealess gene product, Genes Dev. 10, 103-117.
30. Wilk, R., Weizman, I. & Shilo, B.-Z. (1996) Trachealess encodes a bHLH-PAS protein that is an inducer of tracheal cell fates in Drosophila, Genes Dev. 10, 93-102.
31. Nambu, J. R., Chen, W., Hu, S. & Crews, S. T. (1996) The Drosophila melanogaster similar bHLH-PAS gene encodes a protein related to human hypoxia-inducible factor 1 alpha and Drosophila single-minded. Gene (Amst.) 172, 249-254.
32. Hirose, K., Morita, M., Ema, M., Mimura, J., Hamada, H., Fujii, H., Saijo, Y., Gotoh, O., Sogawa, K. & Fujii-Kuriyama, Y. (1996) cDNA cloning and tissue-specific expression of a novel basic helix-loop-helix/PAS factor (Arnt2) with close sequence similarity to the aryl hydrocarbon receptor nuclear translocator (Arnt), Mol. Cell. Biol. 16, 1706-1713.
33. Drutel, G., Kathmann, M., Heron, A., Schwartz, J.-C. & Arrang, J.-M. (1996) Cloning and selective expression in brain and kidney of ARNT2 homologous to the Ah receptor nuclear translocator (ARNT), Biochem. Biophys. Res. Commun. 225, 333-339.
34. Chen, H., Chrast, R., Rossier, C., Gos, A., Antonarakis, S. E., Kudoh, J., Yamaki, A., Shindoh, N., Maeda, H., Minoshima, S. & Shimizu, N. (1995) Single-minded and Down syndrome? Nature Genet. 10, 9-10.
35. Dahmane, N., Charron, G., Lopes, C., Yaspo, M.-L., Maunoury, C., Decorte, L., Sinet, P.-M., Bloch, B. & Delabar, J.-M. (1995) Down syndrome-critical region contains a gene homologous to Drosophila sim expressed during rat and human central nervous system development, Proc. Natl. Sci. USA, 92, 9191-9195.
36. Ema, M., Morita, M., Ikawa, S., Tanaka, M., Matsuda, Y., Gotoh, O., Saijoh, Y., Fujii, H., Hamada, H., Kikuchi, Y. & Fujii-Kuriyama, Y. (1996) Two new members of the murine sim gene family are transcriptional repressor and show different expression patterns during mouse embryogenesis, Mol. Cell. Biol. 16, 5865-5875.
37. Fan, C.-M., Kuwana, E., Bulfone, A., Fletcher, C. F., Copeland, N. G., Jenkins, N. A., Crews, S., Martinez, S., Puelles, L., Rubenstein, J. L. R. & Tessier-Lavigne, M. (1996) Expression patterns of two murine homologs of Drosophila single-minded suggest possible roles in embryonic patterning and in the pathogenesis of Down syndrome, Mol. Cell. Neurosci. 7, 1-16.
38. Moffett, P., Dayo, M., Reece, M., McCormick, M. K. & Pelletier, J. (1996) Characterization of msim, a murine homologue of the Drosophila sim transcription factor, Genomics 35, 144-155.
39. Yamaki, A., Noda, S., Kudoh, J., Shindoh, N., Maeda, H., Minoshima, S., Kawasaki, K., Shimizu, Y. & Shimizu, N. (1996) The mammalian single-minded (SIM) gene: mouse cDNA structure and diencephalic expression indicate a candidate gene for Down syndrome, Genomics 35, 136-143.
40. Gradin, K., McGuire, J., Wenger, R. H., Kvietikova, I., Whitelaw, M. L., Toftgard, R., Tora, L., Gassmann, M. & Poellinger, L. (1996) Functional interference between hypoxia and dioxin signal transduction pathways: competition for recruitment of the Arnt transcription factor, Mol. Cell. Biol. 16, 5221-5231.
41. Jiang, B.-H., Rue, E., Wang, G. L., Roe, R. & Semenza, G. L. (1996) Dimerization, DNA binding and transactivating properties of hypoxia-inducible factor 1, J. Biol. Chem. 271, 17771-17778.
42. Wood, S. M., Gleadle, J. M., Pugh, C. W., Hankinson, O. & Ratcliffe, P. J. (1996) The role of the aryl hydrocarbon receptor nuclear translocalor (ARNT) in hypoxic induction of gene expression, J. Biol. Chem. 271, 15117-15123.
43. Gassmann, M., Kvietikova, I., Rolfs, A. & Wenger, R. H. (1997) Oxygen- and dioxin-regulated gene expression in mouse hepatoma cells, Kidney Int. 51, 567-574.
44. 2 tension, Am. J. Physiol. 271, C1172-C1180.
45. Wiener, C. M., Booth, G. & Semenza, G. L. (1996) In vivo expression of mRNAs encoding hypoxia-inducible factor 1, Biochem. Biophys. Res. Commun. 225, 485-488.
46. Wenger, R. H., Rolfs, A., Marti, H. H., Guénet, J.-L. & Gassmann, M. (1996) Nucleotide sequence, chromosomal assignment and mRNA expression of mouse hypoxia-inducible factor 1α, Biochem. Biophys. Res. Commun. 223, 54-59.
47. Wenger, R. H., Kvietikova, I., Rolfs, A., Gassmann, M. & Marti, H. H. (1997) The hypoxia-inducible factor-1α is regulated at the post-mRNA level, Kidney Int. 51, 560-563.
48. Huang, L. E., Arany, Z., Livingston, D. M. & Bunn, H. F. (1996) Activation of hypoxia-inducible transcription factor depends primarily upon redox-sensitive stabilisation of its α subunit. J. Biol. Chem. 271, 32253-32259.
49. Wang, G. L., Jiang, B.-H. & Semenza, G. L. (1995) Effect of protein kinase and phosphatase inhibitors on expression of hypoxia-inducible factor 1, Biochem. Biophys. Res. Commun. 216, 669-675.
50. Wang, G. L., Jiang, B.-H. & Semenza, G. L. (1995) Effect of altered redox states on expression and DNA-binding activity of hypoxia-inducible factor 1, Biochem. Biophys. Res. Commun. 212, 550-556.
51. Semenza, G. L., Rue, E. A., Iyer, N. V., Pang, M. G. & Kearns, W. G. (1996) Assignment of the hypoxia-inducible factor 1α gene to a region of conserved synteny on mouse chromosome 12 and human chromosome 14q, Genomics 34, 437-439.
52. Sambrook, J., Fritsch, E. F. & Maniatis, T. (1989) Molecular cloning: a laboratory manual, 2nd edn, Cold Spring Harbor Laboratory, Cold Spring Harbor NY.
53. Kvietikova, I., Wenger, R. H., Marti, H. H. & Gassmann, M. (1995) The transcription factors ATF-1 and CREB-1 bind constitutively to the hypoxia-inducible factor-1 (HIF-1) DNA recognition site, Nucleic Acids Res. 23, 4542-4550.
54. Ausubel, F. M., Brent, R., Kingston, R. E., Moore, D. D., Seidman, J. G., Smith, J. A. & Struhl, K. (1989) Current protocols in molecular biology, J. Wiley & Sons, NY.
55. Chomczynski, P. & Sacchi, N. (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction, Anal. Biochem. 162, 156-159.
56. Mount, S. M. (1982) A catalogue of splice junction sequences, Nucleic Acids Res. 10, 459-472.
57. Propst, F. & Vande Woude, G. F. (1984) A novel transposon-like repeat interrupted by an LTR element occurs in a cluster of B1 repeats in the mouse c-mos locus, Nucleic Acids Res. 12, 8381-8392.
58. Krayev, A. S., Markusheva, T. V., Kramerov, D. A., Ryskov, A. P., Skryabin, K. G., Bayev, A. A. & Georgiev, G. P. (1982) Ubiquitous transposon-like repeats B1 and B2 of the mouse genome: B2 sequencing, Nucleic Acids Res. 10, 7461-7475.
59. Bucher, P. (1990) Weight matrix descriptions of tour eukaryotic RNA polymerase II promoter elements derived from 502 unrelated promoter sequences, J. Mol. Biol. 212, 563-578.
60. Kozak, M. (1991) An analysis of vertebrate mRNA sequences: intimations of translational control, J. Cell Biol. 115, 887-903.
61. Devereux, J., Haeberli, P. & Smithies, O. (1984) A comprehensive set of sequence analysis programs for the VAX, Nucleic Acids Res. 12, 387-395.
62. Schichman, S. A., Severynse, D. M., Edgell, M. H. & Hutchison, C. A. III (1992) Strand-specific LINE-1 transcription in mouse F9 cells originates from the youngest phylogenetic subgroup of LINE-1 elements, J. Mol. Biol. 224, 559-574.
63. Burbach, K. M., Poland, A. & Bradfield, C. A. (1992) Cloning of the Ah-receptor cDNA reveals a distinctive ligand-activated transcription factor, Proc. Natl Acad. Sci. USA 89, 8185-8189.
64. Ohno, S. & Epplen, J. T. (1983) The primitive code and repeats of base oligomers as the primordial protein-encoding sequence, Proc. Natl Acad. Sci. USA 80, 3391-3395.
65. Singh, L., Phillips, C. & Jones, K. W. (1984) The conserved nucleotide sequences of Bkm, which define Sxr in the mouse, are transcribed, Cell 36, 111-120.
66. Schmidt, J. V., Carver, L. A. & Bradfield, C. A. (1993) Molecular characterization of the murine Ahr gene. Organization, promoter analysis, and chromosomal assignment, J. Biol. Chem. 268, 22203-22209.
67. Citri, Y., Colot, H. V., Jacquier, A. C., Yu, Q., Hall, J. C., Baltimore, D. & Rosbash, M. (1987) A family of unusually spliced biologically active transcripts encoded by a Drosophila clock gene, Nature 326, 42-47.
68. Muralidhar, M. G., Callahan, C. A. & Thomas, J. B. (1993) Single-minded regulation of genes in the embryonic midline of the Drosophila central nervous system, Mech. Dev. 41, 129-138.
69. Gardiner-Garden, M. & Frommer, M. (1987) CpG islands in vertebrate genomes, J. Mol. Biol. 196, 261-282.