Decreased differentiation of erythroid cells exacerbates ineffective erythropoiesis in β-thalassemia

Blood

Volumn 112, Issue 3, 2008, Pages 875-885

  Libani, Ilaria V ^a,b   Guy, Ella C ^a   Melchiori, Luca ^a   Schiro, Raffaella ^a   Ramos, Pedro ^a,c   Breda, Laura ^a   Scholzen, Thomas ^d   Chadburn, Amy ^e   Liu, Yifang ^e   Kernbach, Margrit ^d   Baron Lühr, Bettina ^d   Porotto, Matteo ^a   De Sousa, Maria ^c   Rachmilewitz, Eliezer A ^f   Hood, John D ^g   Cappellini, M Domenica ^b   Giardina, Patricia J ^a   Grady, Robert W ^a   Gerdes, Johannes ^d   Rivella, Stefano ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b UNIVERSITY OF MILAN   (Italy)

^c UNIVERSITY OF PORTO   (Portugal)

^d RESEARCH CENTER BORSTEL   (Germany)

^e Department of Molecular Biology and Genetics   (United States)

^f Institute of Hematology   (Israel)

^g TargeGen   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN A; CYCLIN DEPENDENT KINASE 2; ERYTHROPOIETIN RECEPTOR; JANUS KINASE 2; JANUS KINASE INHIBITOR; KI 67 ANTIGEN; PROTEIN BCL XL; TG 101209; UNCLASSIFIED DRUG; CYCLIN DEPENDENT KINASE; JAK2 PROTEIN, MOUSE;

ANEMIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BETA THALASSEMIA; CELL CYCLE S PHASE; CELL DIFFERENTIATION; CELL MATURATION; CELL PROLIFERATION; CELL STRUCTURE; CELL SURVIVAL; CONTROLLED STUDY; ERYTHROBLAST; ERYTHROID CELL; ERYTHROPOIESIS; HEMOLYSIS; HUMAN; HUMAN CELL; IN VITRO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPLEEN SIZE; SPLENOMEGALY; ANIMAL; BLOOD; DRUG ANTAGONISM; GENETICS; PATHOLOGY; SPLEEN;

ANIMALS; APOPTOSIS; BETA-THALASSEMIA; CELL DIFFERENTIATION; CYCLIN-DEPENDENT KINASES; ERYTHROID CELLS; ERYTHROPOIESIS; JANUS KINASE 2; MICE; SPLEEN;

EID: 50949133924     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2007-12-126938     Document Type: Article

References (62)

1. Cooley TB, Lee P. A series of cases of splenomegaly in children with anemia and peculiar bone changes. Trans Am Pediatr Soc. 1925;37:29.
2. Weatherall DJ. Single gene disorders or complex traits: lessons from the thalassaemias and other monogenic diseases. BMJ. 2000;321:1117-1120.
3. Weatherall DJ. Phenotype-genotype relationships in monogenic disease: lessons from the thalassaemias. Nat Rev Genet. 2001;2:245-255.
4. Steinberg MH, Forget BG, Higgs DR, Nagel RL. Disorders of Hemoglobin: Genetics, Pathophysiology and Clinical Management. Cambridge, United Kingdom: Cambridge University Press; 2001.
5. Thein SL. Pathophysiology of {beta} thalassemia: a guide to molecular therapies. Hematology (Am Soc Hematol Educ Program). 2005:31-37.
6. Mathias LA, Fisher TC, Zeng L, et al. Ineffective erythropoiesis in beta-thalassemia major is dueto apoptosis at the polychromatophilic normoblast stage. Exp Hematol. 2000;28:1343-1353.
7. Ellis J, Pannell D. The beta-globin locus control region versus gene therapy vectors: a struggle for expression. Clin Genet. 2001;59:17-24.
8. Yuan J, Angelucci E, Lucarelli G, et al. Accelerated programmed cell death (apoptosis) in erythroid precursors of patients with severe betathalassemia (Cooley's anemia). Blood. 1993;82:374-377.
9. Schrier SL. Pathophysiology of thalassemia. Curr Opin Hematol. 2002;9:123-126.
10. Pootrakul P, Sirankapracha P, Hemsorach S, et al. A correlation of erythrokinetics, ineffective erythropoiesis, and erythroid precursor apoptosis in Thai patients with thalassemia. Blood. 2000;96:2606-2612.
11. Kong Y, Zhou S, Kihm AJ, et al. Loss of alphahemoglobin-stabilizing protein impairs erythropoiesis and exacerbates beta-thalassemia. J Glin Invest. 2004;114:1457-1466.
12. Yuan J, Bunyaratvej A, Fucharoen S, Fung C, Shinar E, Schrier SL. The instability of the membrane skeleton in thalassemic red blood cells. Blood. 1995;86:3945-3950.
13. Kuypers FA, Yuan J, Lewis RA, et al. Membrane phospholipid asymmetry in human thalassemia. Blood. 1998;91:3044-3051.
14. Finch CA, Deubelbeiss K, Cook JD, et al. Ferrokinetics in man. Medicine. 1970;49:17-53.
15. Finch CA, Sturgeon P. Erythrokinetics in Cooley's anemia. Blood. 1957;12:64-73.
16. Gentis F, Tabellini L, Lucarelli G, et al. The importance of erythroid expansion in determining the extent of apoptosis in erythroid precursors in patients with beta-thalassemia major. Blood. 2000;96:3624-3629.
17. Angelucci E, Muretto P, NicolucciA, et al. Effects of iron overload and hepatitis C virus positivity in determining progression of liver fibrosis in thalassemia following bone marrow transplantation. Blood. 2002;100:17-21.
18. Bannerman RM, Keusch G, Kreimer-Birnbaum M, Vance VK, Vaughan S. Thalassemia intermedia, with iron overload, cardiac failure, diabetes mellitus, hypopituitarism and porphyrinuria. Am J Med. 1967;42:476-486.
19. Heinrich HC, Gabbe EE, Oppitz KH, et al.Absorption of inorganic and food iron in children with heterozygous and homozygous betathalassemia. Z Kinderheilkd. 1973;115:1-22.
20. Cossu P, Toccafondi C, Vardeu F, et al. Iron overload and desferrioxamine chelation therapy in beta-thalassemia intermedia. Eur J Pediatr. 1981;137:267-271.
21. Fiorelli G, Fargion S, Piperno A, Battafarano N, Cappellini MD. Iron metabolism in thalassemia intermedia. Haematologica. 1990;75:89-95.
22. Gardenghi S, Marongiu MF, Ramos P, et al. Ineffective erythropoiesis in {beta}-thalassemia is characterized by increased iron absorption mediated by down-regulation of hepcidin and upregulation of ferroportin. Blood. 2007;109:5027-5035.
23. Pinto JP, Ribeiro S, Pontes H, et al. Erythropoietin mediates hepcidin expression in hepatocytes through EPOR signalling and regulation of C/EBPα. Blood. 2008;111:5727-5733.
24. Breda L, Gardeng S, Guy E, et al. Exploring the role of hepcidin, an antimicrobial and iron regulatory peptide, in increased iron absorption in {beta}-thalassemia. Ann N YAcad Sei. 2005;1054:417-422.
25. Adamsky K, Weizer O, Amariglio N, et al. Decreased hepcidin mRNA expression in thalassemic mice. Br J Haematol. 2004;124:123-124.
26. Weizer-Stern O, Adamsky K, Breda L, et al. Down regulation of hepcidin and haeniojuvelin expression in the hepatocyte cell line HepG2 induced by thalassaemicsera. BrJ Haematol. 2006;135:129-138.
27. Yang B, Kirby S, Lewis J, Detloff PJ, Maeda N, Smithies O. A mouse model for beta 0-thalassemia. Proc Natl Acad Sci USA. 1995;92:11608-11612.
28. Ciavatta DJ, Ryan TM, Farmer SC, Townes TM. Mouse model of human beta zero thalassemia: targeted deletion of the mouse beta maj- and beta min-globin genes in embryonic stem cells. Proc Natl Acad Sci U SA. 1995;92:9259-9263.
29. Rivella S, May C, Chadburn A, Riviere I, Sadelain M. A novel murine model of Cooley anemia and its rescue by lentiviral-mediated human beta-globin gene transfer. Blood. 2003;101:2932-2939.
30. May C, Rivella S, Chadburn A, Sadelain M. Successful treatment of murine beta-thalassemia intermedia by transfer of the human beta-globin gene. Blood. 2002;99:1902-1908.
31. Wu H, Liu X, Jaenisch R, Lodish HF. Generation of committed erythroid BFU-E and CFU-E progenitors does not require erythropoietin or the erythropoietin receptor. Cell. 1995;83:59-67.
32. D'Andrea A, Fasman G, Wong G, Lodish H. Erythropoietin receptor: cloning strategy and structural features, lnt J Cell Cloning. 1990; 8(suppl 1):173-180.
33. D'Andrea AD, Lodish HF, Wong GG. Expression cloning of the murine erythropoietin receptor. Cell. 1989;57:277-285.
34. Fang J, Menon M, Kapelle W, et al. EPO modulation of cell-cycle regulatory genes, and cell division, in primary bone marrow erythroblasts. Blood. 2007;110:2361-2370.
35. Socolovsky M, Murrell M, Liu Y, Pop R, Porpiglia E, Levchenko A. Negative autoregulation by FAS mediates robust fetal erythropoiesis. PLoS Biol. 2007:5:e252.
36. Menon M P, Karur V, Bogacheva O, Bogachev O, Cuetara B, Wojchowski DM. Signals for stress erythropoiesis are integrated via an erythropoietin receptor-phosphotyrosine-343-Stat5 axis. J Clin Invest. 2006;116:683-694.
37. Dolznig H, Grebien F, Deiner EM, et al. Erythroid progenitor renewal versus differentiation: genetic evidence for cell autonomous, essential functions of EpoR, Stat5 and the GR. Oncogene. 2006;25: 2890-2900.
38. Socolovsky M, Nam H, Fleming MD, HaaseVH, Brugnara C, Lodish HF. Ineffective erythropoiesis in Stat5a(-/-)5b(-/-) mice due to decreased survival of early erythroblasts. Blood. 2001;98:3261-3273.
39. Socolovsky M, Fallon AE, Wang S. Brugnara C. Lodish HF. Fetal anemia and apoptosis of red cell progenitors in Stat5a-/-5b-/- mice: a direct role for Stat5 in BcI-X(L) induction. Cell. 1999;98:181-191.
40. Wagner KU, Claudio E, Rucker EB III, et al. Conditional deletion of the Bcl-x gene from erythroid cells results in hemolytic anemia and profound splenomegaly. Development. 2000;127:4949-4958.
41. Rhodes MM, Kopsombut P, Bondurant MC, Price JO, Koury MJ. Bcl-x(L) prevents apoptosis of late-stage erythroblasts but does not mediate the antiapoptotic effect of erythropoietin. Blood. 2005;106:1857-1863.
42. Socolovsky M. Molecular insights into stress erythropoiesis. Curr Opin Hematol. 2007;14:215-224.
43. Rivella S, Sadelain M. Therapeutic globin gene delivery using lentiviral vectors. Curr Opin Mol Ther. 2002;4:505-514.
44. Boggs DR. The total marrow mass of the mouse: a simplified method of measurement. Am J Hematol. 1984;16:277-286.
45. Ataga KI, Cappellini MD, Rachmilewitz EA. Beta-thalassaemia and sickle cell anaemia as paradigms of hypercoagulability. Br J Haematol. 2007;139:3-13.
46. Richmond TD, Chohan M, Barber DL. Turning cells red: signal transduction mediated by erythropoietin. Trends Cell Biol. 2005;15:146-155.
47. Ihle JN. The Stat family in cytokine signaling. Curr Opin Cell Biol. 2001;13:211-217.
48. TakeharaT Takahashi H. Suppression of Bcl-xL deamidation in human hepatocellular carcinomas. Cancer Res. 2003;63:3054-3057.
49. Traut W, Endl E, ScholzenT, Gerdes J, Winking H. The temporal and spatial distribution of the proliferation associated Ki-67 protein during female and male meiosis. Chromosoma. 2002;111:156-164.
50. Endl E, Kausch I, Baack M, Knippers R, Gerdes J, Scholzen T The expression of Ki-67, MCM3, and p27 defines distinct subsets of proliferating, resting, and differentiated cells. J Pathol. 2001;195:457-462.
51. Popp RA, Popp DM, Johnson FM. Skow LC, Lewis SE. Hematology of a murine beta-thalassemia: a longitudinal study. Ann N Y Acad Sci. 1985;445:432-444.
52. Beauchemin H, Blouin MJ, Trudel M. Differential regulatory and compensatory responses in hematopoiesis/erythropoiesis in alpha- and beta-globin hemizygous mice. J Biol Chem. 2004;279:19471-19480.
53. Neria F, Caramelo C, Peinado H, et al. Mechanisms of endothelial cell protection by blockade of the JAK2 pathway. Am J Physiol Cell Physiol. 2007;292:C1123-C1131.
54. Pardanani A, Hood J, Lasho T, et al. TG101209, a small molecule JAK2-selective kinase inhibitor potently inhibits myeloproliferative disorderassociated JAK2V617F and MPLW515L/K mutations. Leukemia. 2007;21:1658-1668.
55. Wang YL, Vandris K, Jones A, et al. JAK2 mutations are present in all cases of polycythemia vera. Leukemia. 2008;22:1289.
56. Arcasoy MO, Karayal AF, Segal HM, Sinning JG, Forget BG. A novel mutation in the erythropoietin receptor gene is associated with familial erythrocytosis. Blood. 2002;99:3066-3069.
57. Fibach E, Rachmilewitz EA. The two-step liquid culture: a novel procedure for studying maturation of human normal and pathological erythroid precursors. Stem Cells. 1993;11(suppl 1):36-41.
58. Kean LS, Brown LE, Nichols JW, Mohandas N, Archer DR, Hsu LL. Comparison of mechanisms of anemia in mice with sickle cell disease and beta-thalassemia: peripheral destruction, ineffective erythropoiesis, and phospholipid scramblasemediated phosphatidylserine exposure. Exp Hematol. 2002;30:394-402.
59. Ghaffari S, Kitidis C, Zhao W, et al. AKT induces erythroid-cell maturation of JAK2-deficient fetal liver progenitor cells and is required for Epo regulation of erythroid-cell differentiation. Blood. 2006;107:1888-1891.
60. Marinkovic D, Zhang X, Yalcin S, et al. Foxo3 is required for the regulation of oxidative stress in erythropoiesis. J Clin Invest. 2007;117:2133-2144.
61. Arcasoy MO, Jiang X. Co-operative signalling mechanisms required for erythroid precursor expansion in response to erythropoietin and stem cell factor. BrJ Haematol. 2005;130:121-129.
62. Zitnik G, Peterson K, Stamatoyannopoulos G, Papayannopoulou T Effects of butyrate and glucocorticoids on gamma- to beta-globin gene switching in somatic cell hybrids [published erratum appears in Mol Cell Biol. 1995;15:3461]. Mol Cell Biol. 1995;15:790-795.