Generation of a genomic reporter assay system for analysis of γ- and β-globin gene regulation

FASEB Journal

Volumn 26, Issue 4, 2012, Pages 1736-1744

  Chan, Kasey S K ^a,b   Xu, Jian ^c,d   Wardan, Hady ^a   McColl, Bradley ^a   Orkin, Stuart ^c,d   Vadolas, Jim ^a  

^a ROYAL CHILDREN'S HOSPITAL   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c BOSTON CHILDREN S HOSPITAL   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Induction of fetal hemoglobin; RNAi

Indexed keywords

BETA GLOBIN; ENHANCED GREEN FLUORESCENT PROTEIN; GAMMA GLOBIN; RED FLUORESCENT PROTEIN;

ANIMAL CELL; ARTICLE; CELL ASSAY; CONTROLLED STUDY; FLUORESCENCE; FLUORESCENCE BASED CELLULAR REPORTER ASSAY; FUNCTIONAL GENOMICS; GENE CONTROL; HOMOLOGOUS RECOMBINATION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; REPORTER GENE;

ANIMALS; BETA-GLOBINS; CARRIER PROTEINS; CELL LINE; FETAL HEMOGLOBIN; FLUORESCENT DYES; GAMMA-GLOBINS; GENE EXPRESSION REGULATION; GENE KNOCKDOWN TECHNIQUES; GENES, REPORTER; GREEN FLUORESCENT PROTEINS; HUMANS; MICE; NUCLEAR PROTEINS; RNA INTERFERENCE; TRANSGENES;

MURINAE;

EID: 84860893776     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.11-199356     Document Type: Article

References (37)

1. Rees, D. C. (2011) The rationale for using hydroxycarbamide in the treatment of sickle cell disease. Haematologica 96, 488 - 491
2. Cokic, V. P., Andric, S. A., Stojilkovic, S. S., Noguchi, C. T., and Schechter, A. N. (2008) Hydroxyurea nitrosylates and activates soluble guanylyl cyclase in human erythroid cells. Blood 111, 1117-1123 (Pubitemid 351213390)
3. Cokic, V. P., Smith, R. D., Beleslin-Cokic, B. B., Njoroge, J. M., Miller, J. L., Gladwin, M. T., and Schechter, A. N. (2003) Hydroxyurea induces fetal hemoglobin by the nitric oxide-dependent activation of soluble guanylyl cyclase. J. Clin. Invest. 111, 231-239 (Pubitemid 36105922)
4. Ley, T. J., DeSimone, J., Noguchi, C. T., Turner, P. H., Schechter, A. N., Heller, P., and Nienhuis, A. W. (1983) 5-Azacytidine increases gamma-globin synthesis and reduces the proportion of dense cells in patients with sickle cell anemia. Blood 62, 370 -380
5. Ley, T. J., DeSimone, J., Anagnou, N. P., Keller, G. H., Humphries, R. K., Turner, P. H., Young, N. S., Keller, P., and Nienhuis, A. W. (1982) 5-azacytidine selectively increases gamma- globin synthesis in a patient with beta thalassemia. N. Engl. J. Med. 307, 1469-1475 (Pubitemid 13238767)
6. Atweh, G. F., Sutton, M., Nassif, I., Boosalis, V., Dover, G. J., Wallenstein, S., Wright, E., McMahon, L., Stamatoyannopoulos, G., Faller, D. V., and Perrine, S. P. (1999) Sustained induction of fetal hemoglobin by pulse butyrate therapy in sickle cell disease. Blood 93, 1790-1797 (Pubitemid 29128478)
7. Fathallah, H., Taher, A., Bazarbachi, A., and Atweh, G. F. (2009) Differences in response to fetal hemoglobin induction therapy in beta-thalassemia and sickle cell disease. Blood Cells Mol. Dis. 43, 58-62
8. Boosalis, M. S., Castaneda, S. A., Trudel, M., Mabaera, R., White, G. L., Lowrey, C. H., Emery, D. W., Mpollo, M. S., Shen, L., Wargin, W. A., Bohacek, R., Faller, D. V., and Perrine, S. P. (2011) Novel therapeutic candidates, identified by molecular modeling, induce gamma-globin gene expression in vivo. Blood Cells Mol. Dis. 47, 107-116
9. Bradner, J. E., Mak, R., Tanguturi, S. K., Mazitschek, R., Haggarty, S. J., Ross, K., Chang, C. Y., Bosco, J., West, N., Morse, E., Lin, K., Shen, J. P., Kwiatkowski, N. P., Gheldof, N., Dekker, J., DeAngelo, D. J., Carr, S. A., Schreiber, S. L., Golub, T. R., and Ebert, B. L. (2010) Chemical genetic strategy identifies histone deacetylase 1 (HDAC1) and HDAC2 as therapeutic targets in sickle cell disease. Proc. Natl. Acad. Sci. U. S. A. 107, 12617-12622
10. Mabaera, R., West, R. J., Conine, S. J., Macari, E. R., Boyd, C. D., Engman, C. A., and Lowrey, C. H. (2008) A cell stress signaling model of fetal hemoglobin induction: what doesn't kill red blood cells may make them stronger. Exp. Hematol. 36, 1057-1072
11. Wilber, A., Hargrove, P. W., Kim, Y. S., Riberdy, J. M., Sankaran, V. G., Papanikolaou, E., Georgomanoli, M., Anagnou, N. P., Orkin, S. H., Nienhuis, A. W., and Persons, D. A. (2011) Therapeutic levels of fetal hemoglobin in erythroid progeny of beta-thalassemic CD34 cells after lentiviral vector-mediated gene transfer. Blood 117, 2817-2826
12. Xu, J., Sankaran, V. G., Ni, M., Menne, T. F., Puram, R. V., Kim, W., and Orkin, S. H. (2010) Transcriptional silencing of γ-globin by BCL11A involves long-range interactions and cooperation with SOX6. Genes Dev. 24, 783-798
13. Sankaran, V. G., Menne, T. F., Xu, J., Akie, T. E., Lettre, G., Van Handel, B., Mikkola, H. K., Hirschhorn, J. N., Cantor, A. B., and Orkin, S. H. (2008) Human fetal hemoglobin expression is regulated by the developmental stage-specific repressor BCL11A. Science 322, 1839-1842
14. Uda, M., Galanello, R., Sanna, S., Lettre, G., Sankaran, V. G., Chen, W., Usala, G., Busonero, F., Maschio, A., Albai, G., Piras, M. G., Sestu, N., Lai, S., Dei, M., Mulas, A., Crisponi, L., Naitza, S., Asunis, I., Deiana, M., Nagaraja, R., Perseu, L., Satta, S., Cipollina, M. D., Sollaino, C., Moi, P., Hirschhorn, J. N., Orkin, S. H., Abecasis, G. R., Schlessinger, D., and Cao, A. (2008) Genome-wide association study shows BCL11A associated with persistent fetal hemoglobin and amelioration of the phenotype of beta-thalassemia. Proc. Natl. Acad. Sci. U. S. A. 105, 1620 -1625
15. Borg, J., Papadopoulos, P., Georgitsi, M., Gutierrez, L., Grech, G., Fanis, P., Phylactides, M., Verkerk, A. J., van der Spek, P. J., Scerri, C. A., Cassar, W., Galdies, R., van Ijcken, W., Ozgur, Z., Gillemans, N., Hou, J., Bugeja, M., Grosveld, F. G., von Lindern, M., Felice, A. E., Patrinos, G. P., and Philipsen, S. (2010) Haploinsufficiency for the erythroid transcription factor KLF1 causes hereditary persistence of fetal hemoglobin. Nat. Genet. 42, 801-805
16. Thein, S. L., Menzel, S., Lathrop, M., and Garner, C. (2009) Control of fetal hemoglobin: new insights emerging from genomics and clinical implications. Hum. Mol. Genet. 18, R216-223
17. Thein, S. L., Menzel, S., Peng, X., Best, S., Jiang, J., Close, J., Silver, N., Gerovasilli, A., Ping, C., Yamaguchi, M., Wahlberg, K., Ulug, P., Spector, T. D., Garner, C., Matsuda, F., Farrall, M., and Lathrop, M. (2007) Intergenic variants of HBS1L-MYB are responsible for a major quantitative trait locus on chromosome 6q23 influencing fetal hemoglobin levels in adults. Proc. Natl. Acad. Sci. U. S. A. 104, 11346-11351 (Pubitemid 47175143)
18. Cui, S., Kolodziej, K. E., Obara, N., Amaral-Psarris, A., Demmers, J., Shi, L., Engel, J. D., Grosveld, F., Strouboulis, J., and Tanabe, O. (2011) Nuclear receptors TR2 and TR4 recruit multiple epigenetic transcriptional corepressors that associate specifically with the embryonic beta-type globin promoters in differentiated adult erythroid cells. Mol. Cell. Biol. 31, 3298 -3311
19. Filipe, A., Li, Q., Deveaux, S., Godin, I., Romeo, P. H., Stamatoy-annopoulos, G., and Mignotte, V. (1999) Regulation of embryonic/ fetal globin genes by nuclear hormone receptors: a novel perspective on hemoglobin switching. EMBO J. 18, 687-697
20. van Dijk, T. B., Gillemans, N., Pourfarzad, F., van Lom, K., von Lindern, M., Grosveld, F., and Philipsen, S. (2010) Fetal globin expression is regulated by Friend of Prmt1. Blood 116, 4349-4352
21. Jane, S. M., Nienhuis, A. W., and Cunningham, J. M. (1995) Hemoglobin switching in man and chicken is mediated by a heteromeric complex between the ubiquitous transcription factor CP2 and a developmentally specific protein. EMBO J. 14, 97-105
22. Howden, S. E., Voullaire, L., Wardan, H., Williamson, R., and Vadolas, J. (2008) Site-specific, Rep-mediated integration of the intact beta-globin locus in the human erythroleukaemic cell line K562. Gene Ther. 15, 1372-1383
23. Vadolas, J., Wardan, H., Orford, M., Voullaire, L., Zaibak, F., Williamson, R., and Ioannou, P. A. (2002) Development of sensitive fluorescent assays for embryonic and fetal hemoglobin inducers using the human beta-globin locus in erythropoietic cells. Blood 100, 4209-4216 (Pubitemid 35396889)
24. Moffat, J., Grueneberg, D. A., Yang, X., Kim, S. Y., Kloepfer, A. M., Hinkle, G., Piqani, B., Eisenhaure, T. M., Luo, B., Grenier, J. K., Carpenter, A. E., Foo, S. Y., Stewart, S. A., Stockwell, B. R., Hacohen, N., Hahn, W. C., Lander, E. S., Sabatini, D. M., and Root, D. E. (2006) A lentiviral RNAi library for human and mouse genes applied to an arrayed viral high-content screen. Cell 124, 1283-1298
25. Lee, E. C., Yu, D., Martinez de Velasco, J., Tessarollo, L., Swing, D. A., Court, D. L., Jenkins, N. A., and Copeland, N. G. (2001) A highly efficient Escherichia coli-based chromosome engineering system adapted for recombinogenic targeting and subcloning of BAC DNA. Genomics 73, 56-65 (Pubitemid 32382387)
26. Singer, D., Cooper, M., Maniatis, G. M., Marks, P. A., and Rifkind, R. A. (1974) Erythropoietic differentiation in colonies of cells transformed by Friend virus. Proc. Natl. Acad. Sci. U. S. A. 71, 2668-2670
27. Cioe, L., McNab, A., Hubbell, H. R., Meo, P., Curtis, P., and Rovera, G. (1981) Differential expression of the globin genes in human leukemia K562(S) cells induced to differentiate by hemin or butyric acid. Cancer Res. 41, 237-243 (Pubitemid 11218822)
28. Sankaran, V. G., Xu, J., Ragoczy, T., Ippolito, G. C., Walkley, C. R., Maika, S. D., Fujiwara, Y., Ito, M., Groudine, M., Bender, M. A., Tucker, P. W., and Orkin, S. H. (2009) Developmental and species-divergent globin switching are driven by BCL11A. Nature 460, 1093-1097
29. Peterson, K. R., Clegg, C. H., Huxley, C., Josephson, B. M., Haugen, H. S., Furukawa, T., and Stamatoyannopoulos, G. (1993) Transgenic mice containing a 248-kb yeast artificial chromosome carrying the human beta-globin locus display proper developmental control of human globin genes. Proc. Natl. Acad. Sci. U. S. A. 90, 7593-7597 (Pubitemid 23249996)
30. Vadolas, J., Wardan, H., Bosmans, M., Zaibak, F., Jamsai, D., Voullaire, L., Williamson, R., and Ioannou, P. A. (2005) Transgene copy number-dependent rescue of murine beta-globin knockout mice carrying a 183 kb human beta-globin BAC genomic fragment. Biochim. Biophys. Acta 1728, 150 -162
31. Skarpidi, E., Vassilopoulos, G., Li, Q., and Stamatoyannopoulos, G. (2000) Novel in vitro assay for the detection of pharmacologic inducers of fetal hemoglobin. Blood 96, 321-326 (Pubitemid 30456488)
32. Migliaccio, G., Di Baldassarre, A., Di Rico, C., Di Noia, A., Nakamoto, B., Cao, H., Skarpidi, E., and Migliaccio, A. R. (2005) Spontaneous switch from Agamma- to beta-globin promoter activity in a stable transfected dual reporter vector. Blood Cells Mol. Dis. 34, 174-180 (Pubitemid 40250494)
33. Saunthararajah, Y., and DeSimone, J. (2004) Clinical studies with fetal hemoglobin-enhancing agents in sickle cell disease. Semin. Hematol. 41, 11-16 (Pubitemid 39458098)
34. Banzon, V., Ibanez, V., Vaitkus, K., Ruiz, M. A., Peterson, K., DeSimone, J., and Lavelle, D. (2011) siDNMT1 increases gamma-globin expression in chemical inducer of dimerization (CID)-dependent mouse betaYAC bone marrow cells and in baboon erythroid progenitor cell cultures. Exp. Hematol. 39, 26-36 e21
35. Yarbro, J. W. (1992) Mechanism of action of hydroxyurea. Semin. Oncol. 19, 1-10
36. Xu, J., Peng, C., Sankaran, V. G., Shao, Z., Esrick, E. B., Chong, B. G., Ippolito, G. C., Fujiwara, Y., Ebert, B. L., Tucker, P. W., and Orkin, S. H. (2011) Correction of sickle cell disease in adult mice by interference with fetal hemoglobin silencing. Science 334, 993-996
37. Sankaran, V. G., Xu, J., Byron, R., Greisman, H. A., Fisher, C., Weatherall, D. J., Sabath, D. E., Groudine, M., Orkin, S. H., Premawardhena, A., and Bender, M. A. (2011) A functional element necessary for fetal hemoglobin silencing. N. Engl. J. Med. 365, 807-814