Hydroxyurea responsiveness in β-thalassemic patients is determined by the stress response adaptation of erythroid progenitors and their differentiation propensity

Haematologica

Volumn 98, Issue 5, 2013, Pages 696-704

  Pourfarzad, Farzin ^a,f   von Lindern, Marieke ^a,f   Azarkeivan, Azita ^b,c   Hou, Jun ^a,d   Kia, Sima Kheradmand ^a   Esteghamat, Fatemehsadat ^a,f   van Ijcken, Wilfred ^a   Philipsen, Sjaak ^a,d   Najmabadi, Hossein ^c,e   Grosveld, Frank ^a,d  

^a ERASMUS MEDICAL CENTER   (Netherlands)

^b HIGH INSTITUTE FOR RESEARCH AND EDUCATION IN TRANSFUSION MEDICINE   (Iran)

^c Kariminejad and Najmabadi Pathology and Genetics Center   (Iran)

^d Netherlands Consortium for Systems Biology   (Netherlands)

^e UNIVERSITY OF SOCIAL WELFARE AND REHABILITATION SCIENCES   (Iran)

^f UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ARF PROTEIN; CYCLIN DEPENDENT KINASE INHIBITOR 2A; CYCLIN DEPENDENT KINASE INHIBITOR 2B; HEMOGLOBIN ALPHA CHAIN; HEMOGLOBIN BETA CHAIN; HEMOGLOBIN F; HEMOGLOBIN GAMMA CHAIN; HYDROXYUREA; PROTEIN BCL XL; TRANSCRIPTION FACTOR FKHRL1; ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR; HEMOGLOBIN A;

APOPTOSIS; ARTICLE; BETA THALASSEMIA; BLOOD CELL COUNT; BLOOD SAMPLING; CELL DEATH; CELL DIFFERENTIATION; CELL STRUCTURE; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; DRUG RESPONSE; ERYTHROBLAST; ERYTHROID PRECURSOR CELL; GENE EXPRESSION; GENE LOCUS; GENE MUTATION; HUMAN; HUMAN CELL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ISOLATION; RNA PURIFICATION; SINGLE NUCLEOTIDE POLYMORPHISM; UPREGULATION; ADAPTATION; BETA-THALASSEMIA; CLUSTER ANALYSIS; CYTOLOGY; DRUG EFFECTS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGICAL STRESS; TREATMENT OUTCOME;

ADAPTATION, BIOLOGICAL; ADP-RIBOSYLATION FACTORS; APOPTOSIS; BETA-THALASSEMIA; CELL DIFFERENTIATION; CLUSTER ANALYSIS; CYCLIN-DEPENDENT KINASE INHIBITOR P15; CYCLIN-DEPENDENT KINASE INHIBITOR P16; ERYTHROID PRECURSOR CELLS; FETAL HEMOGLOBIN; GAMMA-GLOBINS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC LOCI; HEMOGLOBIN A; HUMANS; HYDROXYUREA; STRESS, PHYSIOLOGICAL; TREATMENT OUTCOME;

EID: 84873998720     PISSN: 03906078     EISSN: 15928721     Source Type: Journal    
DOI: 10.3324/haematol.2012.074492     Document Type: Article

References (66)

1. Weatherall DJ, Clegg JB, Higgs DR, Wood WG. The hemoglobinopathies. In: Scriver CR, ed. The Metabolic and Molecular Bases of Inherited Disease. New York, NY: McGraw-Hill. 2001:4571-636.
2. Borgna-Pignatti C, Gamberini MR. Complications of thalassemia major and their treatment. Expert Rev Hematol. 2011; 4(3):353-66.
3. Borgna-Pignatti C, Rugolotto S, De Stefano P, Zhao H, Cappellini MD, Del Vecchio GC, et al. Survival and complications in patients with thalassemia major treated with transfusion and deferoxamine. Haematologica. 2004;89(10):1187-93.
4. Akinsheye I, Alsultan A, Solovieff N, Ngo D, Baldwin CT, Sebastiani P, et al. Fetal hemoglobin in sickle cell anemia. Blood. 2011;118(1):19-27.
5. Perrine SP, Miller BA, Greene MF, Cohen RA, Cook N, Shackleton C, et al. Butryic acid analogues augment gamma globin gene expression in neonatal erythroid progenitors. Bioche Biophys Res Commun. 1987;148(2):694-700.
6. Ley TJ, DeSimone J, Anagnou NP, Keller GH, Humphries RK, Turner PH, et al. 5- azacytidine selectively increases γ-globin synthesis in a patient with β thalassemia. N Engl J Med. 1982;307(24):1469-75.
7. Veith R, Galanello R, Papayannopoulou T, Stamatoyannopoulos G. Stimulation of Fcell production in patients with sickle-cell anemia treated with cytarabine or hydroxyurea. N Engl J Med. 1985;313(25):1571-5.
8. Dixit A, Chatterjee TC, Mishra P, Choudhry DR, Mahapatra M, Tyagi S, et al. Hydroxyurea in thalassemia intermedia--a promising therapy. Ann Hematol. 2005; 84(7):441-6.
9. Ansari SH, Shamsi TS, Ashraf M, Perveen K, Farzana T, Bohray M, et al. Efficacy of hydroxyurea in providing transfusion independence in beta-thalassemia. J Pediatr Hematol Oncol. 2011;33(5):339-43.
10. Karimi M, Haghpanah S, Farhadi A, Yavarian M. Genotype-phenotype relationship of patients with beta-thalassemia taking hydroxyurea: a 13-year experience in Iran. Int J Hematol. 2012;95(1):51-6.
11. Koren A, Levin C, Dgany O, Kransnov T, Elhasid R, Zalman L, et al. Response to hydroxyurea therapy in β-thalassemia. Am J Hematol. 2008;83(5):366-70.
12. Italia KY, Jijina FJ, Merchant R, Panjwani S, Nadkarni AH, Sawant PM, et al. Response to hydroxyurea in β thalassemia major and intermedia: experience in western India. Clin Chim Acta. 2009;407(1-2):10-5.
13. Cokic VP, Andric SA, Stojilkovic SS, Noguchi CT, Schechter AN. Hydroxyurea nitrosylates and activates soluble guanylyl cyclase in human erythroid cells. Blood. 2008;111(3):1117-23.
14. Park JI, Choi HS, Jeong JS, Han JY, Kim IH. Involvement of p38 Kinase in Hydroxyurea-induced Differentiation of K562 Cells. Cell Growth Differ. 2001; 12(9):481-6.
15. Yang YM, Pace B, Kitchens D, Ballas SK, Shah A, Baliga BS. BFU-E colony growth in response to hydroxyurea: Correlation between in vitro and in vivo fetal hemoglobin induction. Am J Hematol. 1997; 56(4):252-8.
16. Panigrahi I, Marwaha RK, Kulkarni K. The expanding spectrum of thalassemia intermedia. Hematology. 2009;14(6):311-4.
17. Ma Q, Wyszynski DF, Farrell JJ, Kutlar A, Farrer LA, Baldwin CT, et al. Fetal hemoglobin in sickle cell anemia: genetic determinants of response to hydroxyurea. Pharmacogenomics J. 2007;7(6):386-94.
18. Bradai M, Abad MT, Pissard S, Lamraoui F, Skopinski L, de Montalembert M. Hydroxyurea can eliminate transfusion requirements in children with severe β-thalassemia. Blood. 2003;102(4):1529-30.
19. Dixit A, Chatterjee TC, Mishra P, Choudhry DR, Mahapatra M, Tyagi S, et al. Hydroxyurea in thalassemia intermedia - a promising therapy. Ann Hematol. 2005; 84(7):441-6.
20. Yavarian M, Karimi M, Bakker E, Harteveld CL, Giordano PC. Response to hydroxyurea treatment in Iranian transfusiondependent β-thalassemia patients. Haematologica. 2004;89(10):1172-8.
21. Bradai M, Pissard S, Abad MT, Dechartres A, Ribeil JA, Landais P, et al. Decreased transfusion needs associated with hydroxyurea therapy in Algerian patients with thalassemia major or intermedia. Transfusion. 2007;47(10):1830-6.
22. Ware RE, Despotovic JM, Mortier NA, Flanagan JM, He J, Smeltzer MP, et al. Pharmacokinetics, pharmacodynamics, and pharmacogenetics of hydroxyurea treatment for children with sickle cell anemia. Blood. 2011;118(18):4985-91.
23. Jison ML, Munson PJ, Barb JJ, Suffredini AF, Talwar S, Logun C, et al. Blood mononuclear cell gene expression profiles characterize the oxidant, hemolytic, and inflammatory stress of sickle cell disease. Blood. 2004;104(1):270-80.
24. Laurance S, Lansiaux P, Pellay FX, Hauchecorne M, Benecke A, Elion J, et al. Differential modulation of adhesion molecule expression by hydroxycarbamide in human endothelial cells from the microand macrocirculation: potential implications in sickle cell disease vasoocclusive events. Haematologica. 2011;96(4):534-42.
25. Gambero S, Canalli AA, Traina F, Albuquerque DM, Saad ST, Costa FF, et al. Therapy with hydroxyurea is associated with reduced adhesion molecule gene and protein expression in sickle red cells with a concomitant reduction in adhesive properties. Eur J Haematol. 2007;78(2):144-51.
26. Laurance S, Pellay FX, Dossou-Yovo OP, Verger E, Krishnamoorthy R, Lapoumeroulie C, et al. Hydroxycarbamide stimulates the production of proinflammatory cytokines by endothelial cells: relevance to sickle cell disease. Pharmacogenet Genomics. 2010;20(4):257-68.
27. Costa FC, da Cunha AF, Fattori A, de Sousa Peres T, Costa GG, Machado TF, et al. Gene expression profiles of erythroid precursors characterise several mechanisms of the action of hydroxycarbamide in sickle cell anaemia. Br J Haematol. 2007;136(2):333-42.
28. Flanagan JM, Steward S, Howard TA, Mortier NA, Kimble AC, Aygun B, et al. Hydroxycarbamide alters erythroid gene expression in children with sickle cell anaemia. Br J Haematol. 2012;157(2):240-8.
29. Najmabadi H, Karimi-Nejad R, Sahebjam S, Pourfarzad F, Teimourian S, Sahebjam F, et al. The β-thalassemia mutation spectrum in the Iranian population. Hemoglobin. 2001; 25(3):285-96.
30. Sutton M, Bouhassira EE, Nagel RL. Polymerase chain reaction amplification applied to the determination of β-like globin gene cluster haplotypes. Am J Hematol. 1989;32(1):66-9.
31. Panigrahi I, Dixit A, Arora S, Kabra M, Mahapatra M, Choudhry VP, et al. Do alpha deletions influence hydroxyurea response in thalassemia intermedia? Hematology. 2005;10(1):61-3.
32. Leberbauer C, Boulme F, Unfried G, Huber J, Beug H, Mullner EW. Different steroids co-regulate long-term expansion versus terminal differentiation in primary human erythroid progenitors. Blood. 2005; 105(1):85-94.
33. van den Akker E, Satchwell TJ, Pellegrin S, Daniels G, Toye AM. The majority of the in vitro erythroid expansion potential resides in CD34(-) cells, outweighing the contribution of CD34(+) cells and significantly increasing the erythroblast yield from peripheral blood samples. Haematologica. 2010;95(9):1594-8.
34. Beug H, Palmieri S, Freudenstein C, Zentgraf H, Graf T. Hormone-dependent terminal differentiation in vitro of chicken erythroleukemia cells transformed by ts mutants of avian erythroblastosis virus. Cell. 1982;28(4):907-19.
35. Bakker WJ, Blazquez-Domingo M, Kolbus A, Besooyen J, Steinlein P, Beug H, et al. FoxO3a regulates erythroid differentiation and induces BTG1, an activator of protein arginine methyl transferase 1. J Cell Biol. 2004;164(2):175-84.
36. Budzowska M, Jaspers I, Essers J, de Waard H, van Drunen E, Hanada K, et al. Mutation of the mouse Rad17 gene leads to embryonic lethality and reveals a role in DNA damage-dependent recombination. EMBO J. 2004;23(17):3548-58.
37. Fibach E, Prasanna P, Rodgers GP, Samid D. Enhanced fetal hemoglobin production by phenylacetate and 4- phenylbutyrate in erythroid precursors derived from normal donors and patients with sickle cell anemia and β-thalassemia. Blood. 1993; 82(7):2203-9.
38. Tusher VG, Tibshirani R, Chu G. Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA. 2001;98(9):5116-21.
39. Minami R, Muta K, Umemura T, Motomura S, Abe Y, Nishimura J, et al. p16(INK4a) induces differentiation and apoptosis in erythroid lineage cells. Exp Hematol. 2003;31(5):355-62.
40. Kheradmand Kia S, Solaimani Kartalaei P, Farahbakhshian E, Pourfarzad F, von Lindern M, Verrijzer CP. EZH2-dependent chromatin looping controls INK4a and INK4b, but not ARF, during human progenitor cell differentiation and cellular senescence. Epigenetics Chromatin. 2009; 2(1):16.
41. Williams RT, Sherr CJ. The INK4-ARF (CDKN2A/B) locus in hematopoiesis and BCR-ABL-induced leukemias. Cold Spring Harb Symp Quant Biol. 2008;73:461-7.
42. Durante W, Johnson FK, Johnson RA. Arginase: a critical regulator of nitric oxide synthesis and vascular function. Clin Exp Pharmacol Physiol. 2007;34(9):906-11.
43. Steinmann S, Schulte K, Beck K, Chachra S, Bujnicki T, Klempnauer KH. v-Myc inhibits C/EBP[β] activity by preventing C/EBP[β]- induced phosphorylation of the co-activator p300. Oncogene. 2009;28(26):2446-55.
44. Yoshida H, Kitabayashi I. Chromatin regulation by AML1 complex. Int J Hematol. 2008;87(1):19-24.
45. Bakker WJ, van Dijk TB, Parren-van Amelsvoort M, Kolbus A, Yamamoto K, Steinlein P, et al. Differential Regulation of Foxo3a Target Genes in Erythropoiesis. Mol Cell Biol. 2007;27(10):3839-54.
46. Døsen-Dahl G, Munthe E, Nygren MK, Stubberud H, Hystad ME, Rian E. Bone marrow stroma cells regulate TIEG1 expression in acute lymphoblastic leukemia cells: role of TGFβ/BMP-6 and TIEG1 in chemotherapy escape. Int J Cancer. 2008;123(12):2759-66.
47. Moucadel V, Constantinescu SN. Differential STAT5 signaling by liganddependent and constitutively active cytokine receptors. J Biol Chem. 2005; 280(14):13364-73.
48. Ranuncolo SM, Polo JM, Dierov J, Singer M, Kuo T, Greally J, et al. Bcl-6 mediates the germinal center B cell phenotype and lymphomagenesis through transcriptional repression of the DNA-damage sensor ATR. Nat Immunol. 2007;8(7):705-14.
49. Blau CA, Constantoulakis P, al-Khatti A, Spadaccino E, Goldwasser E, Papayannopoulou T, et al. Fetal hemoglobin in acute and chronic states of erythroid expansion. Blood. 1993;81(1):227-33.
50. Papayannopoulou T, Vichinsky E, Stamatoyannopoulos G. Fetal Hb production during acute erythroid expansion. I. Observations in patients with transient erythroblastopenia and post-phlebotomy. Br J Haematol. 1980;44(4):535-46.
51. Stamatoyannopoulos G, Veith R, Al-Khatti A, Fritsch EF, Goldwasser E, Papayannopoulou T. On the induction of fetal hemoglobin in the adult; stress erythropoiesis, cell cycle-specific drugs, and recombinant erythropoietin. Prog Clin Biol Res. 1987;251:443-53.
52. Sankaran VG, Lettre G, Orkin SH, Hirschhorn JN. Modifier genes in Mendelian disorders: the example of hemoglobin disorders. Ann N Y Acad Sci. 2010; 1214:47-56.
53. Emambokus N, Vegiopoulos A, Harman B, Jenkinson E, Anderson G, Frampton J. Progression through key stages of haemopoiesis is dependent on distinct threshold levels of c-Myb. EMBO J. 2003; 22(17):4478-88.
54. Rank G, Cerruti L, Simpson RJ, Moritz RL, Jane SM, Zhao Q. Identification of a PRMT5-dependent repressor complex linked to silencing of human fetal globin gene expression. Blood. 2010;116(9):1585-92.
55. Lopez RA, Schoetz S, DeAngelis K, O'Neill D, Bank A. Multiple hematopoietic defects and delayed globin switching in Ikaros null mice. Proc Natl Acad Sci USA. 2002; 99(2):602-7.
56. Boosalis MS, Bandyopadhyay R, Bresnick EH, Pace BS, Van DeMark K, Zhang B, et al. Short-chain fatty acid derivatives stimulate cell proliferation and induce STAT-5 activation. Blood. 2001;97(10):3259-67.
57. Merryweather-Clarke AT, Atzberger A, Soneji S, Gray N, Clark K, Waugh C, et al. Global gene expression analysis of human erythroid progenitors. Blood. 2011; 117(13):e96-108.
58. Hattangadi SM, Lodish HF. Regulation of erythrocyte lifespan: do reactive oxygen species set the clock? J Clin Invest. 2007; 117(8):2075-7.
59. Szekeres T, Fritzer-Szekeres M, Elford HL, Jayaram HM. The Enzyme Ribonucleotide Reductase: Target for Antitumor and Anti- HIV Therapy. Crit Rev Clin Lab Sci. 1997;34(6):503-28.
60. Gumruk F, Tavil B, Balta G, Unal S, Gurgey A. Significance of fetal hemoglobin values in detection of heterozygotes in fanconi anemia: reevaluation of fetal hemoglobin values by a sensitive method. J Pediatr Hematol Oncol. 2008;30(12):896-899
61. Motoyama N, Kimura T, Takahashi T, Watanabe T, Nakano T. bcl-x Prevents Apoptotic Cell Death of Both Primitive and Definitive Erythrocytes at the End of Maturation. J Exp Med 1999;189(11):1691-1618.
62. Cokic VP, Beleslin-Cokic BB, Tomic M, Stojilkovic SS, Noguchi CT, Schechter AN. Hydroxyurea induces the eNOS-cGMP pathway in endothelial cells. Blood. 2006; 108(1):184-191.
63. Lou T, Singh M, Mackie A, Li W, Pace B. Hydroxyurea generates nitric oxide in human erythroid cells: mechanisms for gamma-globin gene activation. Exp Biol Med (Maywood). 2009;234(11):1374-1382.
64. Maciejewski JP, Selleri C, Sato T, Cho HJ, Keefer LK, Nathan CF, et al. Nitric oxide suppression of human hematopoiesis in vitro. Contribution to inhibitory action of interferon-γ and tumor necrosis α. J Clin Invest. 1995;96(2):1085-1092.
65. Kucukkaya B, Arslan DO, Kan B. Role of G proteins and ERK activation in hemininduced erythroid differentiation of K562 cells. Life Sci. 2006;78(11):1217-1224.
66. Calatayud S, Beltrán B, Brines J, Moncada S, Esplugues JV. Foetal erythrocytes exhibit an increased ability to scavenge for nitric oxide. Eur J Pharmacol. 1998;347(2-3):363-366.