Pharmacological Induction of Human Fetal Globin Gene in Hydroxyurea-Resistant Primary Adult Erythroid Cells

REFERENCES

• Weatherall DJ. 2001. Phenotype-genotype relationships in monogenic disease: lessons from the thalassaemias. Nat Rev Genet 2:245–255. http://dx.doi.org/10.1038/35066048.
   PubMed Web of Science ®Google Scholar
• Patrinos GP, Grosveld FG. 2008. Pharmacogenomics and therapeutics of hemoglobinopathies. Hemoglobin 32:229–236. http://dx.doi.org/10.1080/03630260701680367.
   PubMed Web of Science ®Google Scholar
• Schechter AN. 2008. Hemoglobin research and the origins of molecular medicine. Blood 112:3927–3938. http://dx.doi.org/10.1182/blood-2008-04-078188.
   PubMed Web of Science ®Google Scholar
• Bauer DE, Kamran SC, Orkin SH. 2012. Reawakening fetal hemoglobin: prospects for new therapies for the beta-globin disorders. Blood 120:2945–2953. http://dx.doi.org/10.1182/blood-2012-06-292078.
   PubMed Web of Science ®Google Scholar
• Higgs DR, Engel JD, Stamatoyannopoulos G. 2012. Thalassaemia. Lancet 379:373–383. http://dx.doi.org/10.1016/S0140-6736(11)60283-3.
   PubMed Web of Science ®Google Scholar
• Perrine SP, Castaneda SA, Chui DH, Faller DV, Berenson RJ, Siritanaratku N, Fucharoen S. 2010. Fetal globin gene inducers: novel agents and new potential. Ann N Y Acad Sci 1202:158–164. http://dx.doi.org/10.1111/j.1749-6632.2010.05593.x.
   PubMed Web of Science ®Google Scholar
• Natta CL, Niazi GA, Ford S, Bank A. 1974. Balanced globin chain synthesis in hereditary persistence of fetal hemoglobin. J Clin Invest 54:433–438. http://dx.doi.org/10.1172/JCI107779.
   PubMedGoogle Scholar
• Noguchi CT, Rodgers GP, Serjeant G, Schechter AN. 1988. Levels of fetal hemoglobin necessary for treatment of sickle cell disease. N Engl J Med 318:96–99. http://dx.doi.org/10.1056/NEJM198801143180207.
   PubMed Web of Science ®Google Scholar
• Ley TJ, Nienhuis AW. 1985. Induction of hemoglobin F synthesis in patients with beta thalassemia. Annu Rev Med 36:485–498. http://dx.doi.org/10.1146/annurev.me.36.020185.002413.
   PubMed Web of Science ®Google Scholar
• Humphries RK, Dover G, Young NS, Moore JG, Charache S, Ley T, Nienhuis AW. 1985. 5-Azacytidine acts directly on both erythroid precursors and progenitors to increase production of fetal hemoglobin. J Clin Invest 75:547–557. http://dx.doi.org/10.1172/JCI111731.
   PubMed Web of Science ®Google Scholar
• Olivieri NF, Weatherall DJ. 1998. The therapeutic reactivation of fetal haemoglobin. Hum Mol Genet 7:1655–1658. http://dx.doi.org/10.1093/hmg/7.10.1655.
   PubMed Web of Science ®Google Scholar
• McCaffrey PG, Newsome DA, Fibach E, Yoshida M, Su MS. 1997. Induction of gamma-globin by histone deacetylase inhibitors. Blood 90:2075–2083.
   PubMed Web of Science ®Google Scholar
• Witt O, Monkemeyer S, Ronndahl G, Erdlenbruch B, Reinhardt D, Kanbach K, Pekrun A. 2003. Induction of fetal hemoglobin expression by the histone deacetylase inhibitor apicidin. Blood 101:2001–2007. http://dx.doi.org/10.1182/blood-2002-08-2617.
   PubMed Web of Science ®Google Scholar
• Constantoulakis P, Knitter G, Stamatoyannopoulos G. 1989. On the induction of fetal hemoglobin by butyrates: in vivo and in vitro studies with sodium butyrate and comparison of combination treatments with 5-AzaC and AraC. Blood 74:1963–1971.
   PubMed Web of Science ®Google Scholar
• Fucharoen S, Inati A, Siritanaratku N, Thein SL, Wargin WC, Koussa S, Taher A, Chaneim N, Boosalis M, Berenson R, Perrine SP. 2013. A randomized phase I/II trial of HQK-1001, an oral fetal globin gene inducer, in beta-thalassaemia intermedia and HbE/beta-thalassaemia. Br J Haematol 161:587–593. http://dx.doi.org/10.1111/bjh.12304.
   PubMed Web of Science ®Google Scholar
• Grigg A. 2007. Effect of hydroxyurea on sperm count, motility and morphology in adult men with sickle cell or myeloproliferative disease. Intern Med J 37:190–192. http://dx.doi.org/10.1111/j.1445-5994.2006.01290.x.
   PubMed Web of Science ®Google Scholar
• Kinney TR, Helms RW, O'Branski EE, Ohene-Frempong K, Wang W, Daeschner C, Vichinsky E, Redding-Lallinger R, Gee B, Platt OS, Ware RE. 1999. Safety of hydroxyurea in children with sickle cell anemia: results of the HUG-KIDS study, a phase I/II trial. Pediatric Hydroxyurea Group. Blood 94:1550–1554.
   PubMed Web of Science ®Google Scholar
• Steinberg MH, Lu ZH, Barton FB, Terrin ML, Charache S, Dover GJ. 1997. Fetal hemoglobin in sickle cell anemia: determinants of response to hydroxyurea. Multicenter study of hydroxyurea. Blood 89:1078–1088.
   PubMed Web of Science ®Google Scholar
• Atweh G, Fathallah H. 2010. Pharmacologic induction of fetal hemoglobin production. Hematol Oncol Clin North Am 24:1131–1144. http://dx.doi.org/10.1016/j.hoc.2010.08.001.
   PubMed Web of Science ®Google Scholar
• Sankaran VG, Menne TF, Xu J, Akie TE, Lettre G, Van Handel B, Mikkola HK, Hirschhorn JN, Cantor AB, Orkin SH. 2008. Human fetal hemoglobin expression is regulated by the developmental stage-specific repressor BCL11A. Science 322:1839–1842. http://dx.doi.org/10.1126/science.1165409.
   PubMed Web of Science ®Google Scholar
• Zhou W, Clouston DR, Wang X, Cerruti L, Cunningham JM, Jane SM. 2000. Induction of human fetal globin gene expression by a novel erythroid factor, NF-E4. Mol Cell Biol 20:7662–7672. http://dx.doi.org/10.1128/MCB.20.20.7662-7672.2000.
   PubMed Web of Science ®Google Scholar
• Jiang J, Best S, Menzel S, Silver N, Lai MI, Surdulescu GL, Spector TD, Thein SL. 2006. cMYB is involved in the regulation of fetal hemoglobin production in adults. Blood 108:1077–1083. http://dx.doi.org/10.1182/blood-2006-01-008912.
   PubMed Web of Science ®Google Scholar
• Pace B, Qian X, Sangerman J, Oforiacquah S, Baliga B, Han J, Critz S. 2003. p38 MAP kinase activation mediates γ-globin gene induction in erythroid progenitors. Exp Hematol 31:1089–1096. http://dx.doi.org/10.1016/S0301-472X(03)00235-2.
   PubMedGoogle Scholar
• Ramakrishnan V, Pace BS. 2011. Regulation of gamma-globin gene expression involves signaling through the p38 MAPK/CREB1 pathway. Blood Cells Mol Dis 47:12–22. http://dx.doi.org/10.1016/j.bcmd.2011.03.003.
   PubMed Web of Science ®Google Scholar
• Forrester WC, Novak U, Gelinas R, Groudine M. 1989. Molecular analysis of the human beta-globin locus activation region. Proc Natl Acad Sci U S A 86:5439–5443. http://dx.doi.org/10.1073/pnas.86.14.5439.
   PubMed Web of Science ®Google Scholar
• Bodine DM, Ley TJ. 1987. An enhancer element lies 3′ to the human A gamma globin gene. EMBO J 6:2997–3004.
   PubMed Web of Science ®Google Scholar
• Singer D, Cooper M, Maniatis GM, Marks PA, Rifkind RA. 1974. Erythropoietic differentiation in colonies of cells transformed by Friend virus. Proc Natl Acad Sci U S A 71:2668–2670. http://dx.doi.org/10.1073/pnas.71.7.2668.
   PubMed Web of Science ®Google Scholar
• Andersson LC, Nilsson K, Gahmberg CG. 1979. K562—a human erythroleukemic cell line. Int J Cancer 23:143–147. http://dx.doi.org/10.1002/ijc.2910230202.
   PubMed Web of Science ®Google Scholar
• Yue QF, Xiong B, Chen WX, Liu XY. 2014. Comparative study of the efficacy of Wright-Giemsa stain and Liu's stain in the detection of Auer rods in acute promyelocytic leukemia. Acta Histochem 116:1113–1116. http://dx.doi.org/10.1016/j.acthis.2014.05.005.
   PubMedGoogle Scholar
• Daftari P, Gavva NR, Shen CK. 1999. Distinction between AP1 and NF-E2 factor-binding at specific chromatin regions in mammalian cells. Oncogene 18:5482–5486. http://dx.doi.org/10.1038/sj.onc.1202916.
   PubMedGoogle Scholar
• Vadolas J, Wardan H, Orford M, Voullaire L, Zaibak F, Williamson R, Ioannou PA. 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. http://dx.doi.org/10.1182/blood-2001-12-0365.
   PubMedGoogle Scholar
• Chan KS, Xu J, Wardan H, McColl B, Orkin S, Vadolas J. 2012. Generation of a genomic reporter assay system for analysis of gamma- and beta-globin gene regulation. FASEB J 26:1736–1744. http://dx.doi.org/10.1096/fj.11-199356.
   PubMedGoogle Scholar
• Xu J, Sankaran VG, Ni M, Menne TF, Puram RV, Kim W, Orkin SH. 2010. Transcriptional silencing of gamma-globin by BCL11A involves long-range interactions and cooperation with SOX6. Genes Dev 24:783–798. http://dx.doi.org/10.1101/gad.1897310.
   PubMed Web of Science ®Google Scholar
• Orkin SH. 1992. GATA-binding transcription factors in hematopoietic cells. Blood 80:575–581.
   PubMed Web of Science ®Google Scholar
• Bulger M, Sawado T, Schubeler D, Groudine M. 2002. ChIPs of the beta-globin locus: unraveling gene regulation within an active domain. Curr Opin Genet Dev 12:170–177. http://dx.doi.org/10.1016/S0959-437X(02)00283-6.
   PubMed Web of Science ®Google Scholar
• Bieker JJ. 2005. Probing the onset and regulation of erythroid cell-specific gene expression. Mt Sinai J Med 72:333–338.
   PubMedGoogle Scholar
• Raich N, Clegg CH, Grofti J, Romeo PH, Stamatoyannopoulos G. 1995. GATA1 and YY1 are developmental repressors of the human epsilon-globin gene. EMBO J 14:801–809.
   PubMed Web of Science ®Google Scholar
• Tanabe O, McPhee D, Kobayashi S, Shen Y, Brandt W, Jiang X, Campbell AD, Chen YT, Chang C, Yamamoto M, Tanimoto K, Engel JD. 2007. Embryonic and fetal beta-globin gene repression by the orphan nuclear receptors, TR2 and TR4 EMBO J 26:2295–2306. http://dx.doi.org/10.1038/sj.emboj.7601676.
   PubMed Web of Science ®Google Scholar
• Gallarda JL, Foley KP, Yang ZY, Engel JD. 1989. The beta-globin stage selector element factor is erythroid-specific promoter/enhancer binding protein NF-E4. Genes Dev 3:1845–1859. http://dx.doi.org/10.1101/gad.3.12a.1845.
   PubMed Web of Science ®Google Scholar
• Chen RL, Chou YC, Lan YJ, Huang TS, Shen CK. 2010. Developmental silencing of human zeta-globin gene expression is mediated by the transcriptional repressor RREB1. J Biol Chem 285:10189–10197. http://dx.doi.org/10.1074/jbc.M109.049130.
   PubMed Web of Science ®Google Scholar
• Xu J, Peng C, Sankaran VG, Shao Z, Esrick EB, Chong BG, Ippolito GC, Fujiwara Y, Ebert BL, Tucker PW, Orkin SH. 2011. Correction of sickle cell disease in adult mice by interference with fetal hemoglobin silencing. Science 334:993–996. http://dx.doi.org/10.1126/science.1211053.
   PubMed Web of Science ®Google Scholar
• Chen Z, Luo HY, Steinberg MH, Chui DH. 2009. BCL11A represses HBG transcription in K562 cells. Blood Cells Mol Dis 42:144–149. http://dx.doi.org/10.1016/j.bcmd.2008.12.003.
   PubMed Web of Science ®Google Scholar
• Weinberg RS, Ji X, Sutton M, Perrine S, Galperin Y, Li Q, Liebhaber SA, Stamatoyannopoulos G, Atweh GF. 2005. Butyrate increases the efficiency of translation of gamma-globin mRNA. Blood 105:1807–1809. http://dx.doi.org/10.1182/blood-2004-02-0454.
   PubMed Web of Science ®Google Scholar
• Yang YM, Pace B, Kitchens D, Ballas SK, Shah A, Baliga BS. 1997. BFU-E colony growth in response to hydroxyurea: correlation between in vitro and in vivo fetal hemoglobin induction. Am J Hematol 56:252–258. http://dx.doi.org/10.1002/(SICI)1096-8652(199712)56:4<252::AID-AJH10>3.0.CO;2-B.
   PubMed Web of Science ®Google Scholar
• Skarpidi E, Vassilopoulos G, Li Q, Stamatoyannopoulos G. 2000. Novel in vitro assay for the detection of pharmacologic inducers of fetal hemoglobin. Blood 96:321–326.
   PubMed Web of Science ®Google Scholar
• Migliaccio G, Di Baldassarre A, Di Rico C, Di Noia A, Nakamoto B, Cao H, Skarpidi E, Migliaccio AR. 2005. Spontaneous switch from Agamma- to beta-globin promoter activity in a stable transfected dual reporter vector. Blood Cells Mol Dis 34:174–180. http://dx.doi.org/10.1016/j.bcmd.2004.11.005.
   PubMedGoogle Scholar
• Nam TG, Lee J, Walker JR, Brinker A, Cho CY, Schultz PG. 2011. Identification and characterization of small-molecule inducers of fetal hemoglobin. ChemMedChem 6:777–780. http://dx.doi.org/10.1002/cmdc.201000505.
   PubMedGoogle Scholar
• Pace BS, White GL, Dover GJ, Boosalis MS, Faller DV, Perrine SP. 2002. Short-chain fatty acid derivatives induce fetal globin expression and erythropoiesis in vivo. Blood 100:4640–4648. http://dx.doi.org/10.1182/blood-2002-02-0353.
   PubMed Web of Science ®Google Scholar
• Constantoulakis P, Papayannopoulou T, Stamatoyannopoulos G. 1988. α-Amino-N-butyric acid stimulates fetal hemoglobin in the adult. Blood 72:1961–1967.
   PubMed Web of Science ®Google Scholar
• Liakopoulou E, Blau CA, Li Q, Josephson B, Wolf JA, Fournarakis B, Raisys V, Dover G, Papayannopoulou T, Stamatoyannopoulos G. 1995. Stimulation of fetal hemoglobin production by short chain fatty acids. Blood 86:3227–3235.
   PubMed Web of Science ®Google Scholar
• Inati A, Kahale M, Perrine SP, Chui DH, Taher AT, Koussa S, Abi Nasr T, Abbas HA, Ghalie RG. 2014. A phase 2 study of HQK-1001, an oral fetal haemoglobin inducer, in beta-thalassaemia intermedia. Br J Haematol 164:456–458. http://dx.doi.org/10.1111/bjh.12635.
   PubMed Web of Science ®Google Scholar
• Kutlar A, Reid ME, Inati A, Taher AT, Abboud MR, El-Beshlawy A, Buchanan GR, Smith H, Ataga KI, Perrine SP, Ghalie RG. 2013. A dose-escalation phase IIa study of 2,2-dimethylbutyrate (HQK-1001), an oral fetal globin inducer, in sickle cell disease. Am J Hematol 88:E255–E260. http://dx.doi.org/10.1002/ajh.23533.
   PubMed Web of Science ®Google Scholar
• Patthamalai P, Fuchareon S, Chaneiam N, Ghalie RG, Chui DH, Boosalis MS, Perrine SP. 2014. A phase 2 trial of HQK-1001 in HbE-beta thalassemia demonstrates HbF induction and reduced anemia. Blood 123:1956–1957. http://dx.doi.org/10.1182/blood-2013-11-538470.
   PubMed Web of Science ®Google Scholar
• Reid ME, El Beshlawy A, Inati A, Kutlar A, Abboud MR, Haynes J, Jr, Ward R, Sharon B, Taher AT, Smith W, Manwani D, Ghalie RG. 2014. A double-blind, placebo-controlled phase II study of the efficacy and safety of 2,2-dimethylbutyrate (HQK-1001), an oral fetal globin inducer, in sickle cell disease. Am J Hematol 89:709–713. http://dx.doi.org/10.1002/ajh.23725.
   PubMed Web of Science ®Google Scholar
• Cokic VP, Smith RD, Beleslin-Cokic BB, Njoroge JM, Miller JL, Gladwin MT, Schechter AN. 2003. Hydroxyurea induces fetal hemoglobin by the nitric oxide-dependent activation of soluble guanylyl cyclase. J Clin Invest 111:231–239. http://dx.doi.org/10.1172/JCI16672.
   PubMed Web of Science ®Google Scholar
• Lou TF, Singh M, Mackie A, Li W, Pace BS. 2009. Hydroxyurea generates nitric oxide in human erythroid cells: mechanisms for gamma-globin gene activation. Exp Biol Med (Maywood, NJ) 234:1374–1382. http://dx.doi.org/10.3181/0811-RM-339.
   PubMed Web of Science ®Google Scholar
• Huwiler A, Pfeilschifter J. 1999. Nitric oxide stimulates the stress-activated protein kinase p38 in rat renal mesangial cells. J Exp Biol 202:655–660.
   PubMedGoogle Scholar
• Park JI, Choi HS, Jeong JS, Han JY, Kim IH. 2001. Involvement of p38 kinase in hydroxyurea-induced differentiation of K562 cells. Cell Growth Differ 12:481–486.
   PubMedGoogle Scholar
• Witt O, Sand K, Pekrun A. 2000. Butyrate-induced erythroid differentiation of human K562 leukemia cells involves inhibition of ERK and activation of p38 MAP kinase pathways. Blood 95:2391–2396.
   PubMed Web of Science ®Google Scholar
• Mabaera R, West RJ, Conine SJ, Macari ER, Boyd CD, Engman CA, Lowrey CH. 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. http://dx.doi.org/10.1016/j.exphem.2008.06.014.
   PubMed Web of Science ®Google Scholar
• Sankaran VG, Xu J, Ragoczy T, Ippolito GC, Walkley CR, Maika SD, Fujiwara Y, Ito M, Groudine M, Bender MA, Tucker PW, Orkin SH. 2009. Developmental and species-divergent globin switching are driven by BCL11A. Nature 460:1093–1097. http://dx.doi.org/10.1038/nature08243.
   PubMed Web of Science ®Google Scholar
• Zhou D, Liu K, Sun CW, Pawlik KM, Townes TM. 2010. KLF1 regulates BCL11A expression and gamma- to beta-globin gene switching. Nat Genet 42:742–744. http://dx.doi.org/10.1038/ng.637.
   PubMed Web of Science ®Google Scholar
• Platt OS, Thorington BD, Brambilla DJ, Milner PF, Rosse WF, Vichinsky E, Kinney TR. 1991. Pain in sickle cell disease. Rates and risk factors. N Engl J Med 325:11–16.
   PubMed Web of Science ®Google Scholar
• Platt OS, Brambilla DJ, Rosse WF, Milner PF, Castro O, Steinberg MH, Klug PP. 1994. Mortality in sickle cell disease. Life expectancy and risk factors for early death. N Engl J Med 330:1639–1644.
   PubMed Web of Science ®Google Scholar
• Powars DR, Weiss JN, Chan LS, Schroeder WA. 1984. Is there a threshold level of fetal hemoglobin that ameliorates morbidity in sickle cell anemia? Blood 63:921–926.
   PubMed Web of Science ®Google Scholar
• Lebensburger JD, Pestina TI, Ware RE, Boyd KL, Persons DA. 2010. Hydroxyurea therapy requires HbF induction for clinical benefit in a sickle cell mouse model. Haematologica 95:1599–1603. http://dx.doi.org/10.3324/haematol.2010.023325.
   PubMed Web of Science ®Google Scholar